Air-sea carbon dioxide equilibrium: Will it be possible to use seaweeds for carbon removal offsets?

To limit global warming below 2°C by 2100, we must drastically reduce greenhouse gas emissions and additionally remove ~100-900 Gt CO2 from the atmosphere (carbon dioxide removal, CDR) to compensate for unavoidable emissions. Seaweeds (marine macroalgae) naturally grow in coastal regions worldwide where they are crucial for primary production and carbon cycling. They are being considered as a biological method for CDR and for use in carbon trading schemes as offsets. To use seaweeds in carbon trading schemes requires verification that seaweed photosynthesis that fixes CO2 into organic carbon results in CDR, along with the safe and secure storage of the carbon removed from the atmosphere for more than 100 years (sequestration). There is much ongoing research into the magnitude of seaweed carbon storage pools (e.g., as living biomass and as particulate and dissolved organic carbon in sediments and the deep ocean), but these pools do not equate to CDR unless the amount of CO2 removed from the atmosphere as a result of seaweed primary production can be quantified and verified. The draw-down of atmospheric CO2 into seawater is via air-sea CO2 equilibrium, which operates on time scales of weeks to years depending upon the ecosystem considered. Here, we explain why quantifying air-sea CO2 equilibrium and linking this process to seaweed carbon storage pools is the critical step needed to verify CDR by discrete seaweed beds and nearshore and open ocean aquaculture systems prior to their use in carbon trading.

Standing genetic variation fuels rapid adaptation to ocean acidification.

Global climate change has intensified the need to assess the capacity for natural populations to adapt to abrupt shifts in the environment. Reductions in seawater pH constitute a conspicuous global change stressor that is affecting marine ecosystems globally. Here, we quantify the phenotypic and genetic modifications associated with rapid adaptation to reduced seawater pH in the Mediterranean mussel, Mytilus galloprovincialis. We reared a genetically diverse larval population in two pH treatments (pHT 8.1 and 7.4) and tracked changes in the shell-size distribution and genetic variation through settlement. Additionally, we identified differences in the signatures of selection on shell growth in each pH environment. Both phenotypic and genetic data show that standing variation can facilitate adaptation to declines in seawater pH. This work provides insight into the processes underpinning rapid evolution, and demonstrates the importance of maintaining variation within natural populations to bolster species' adaptive capacity as global change progresses.

Ocean pH fluctuations affect mussel larvae at key developmental transitions.

Coastal marine ecosystems experience dynamic fluctuations in seawater carbonate chemistry. The importance of this variation in the context of ocean acidification requires knowing what aspect of variability biological processes respond to. We conducted four experiments (ranging from 3 to 22 days) with different variability regimes (pHT 7.4-8.1) assessing the impact of diel fluctuations in carbonate chemistry on the early development of the mussel Mytilus galloprovincialis. Larval shell growth was consistently correlated to mean exposures, regardless of variability regimes, indicating that calcification responds instantaneously to seawater chemistry. Larval development was impacted by timing of exposure, revealing sensitivity of two developmental processes: development of the shell field, and transition from the first to the second larval shell. Fluorescent staining revealed developmental delay of the shell field at low pH, and abnormal development thereof was correlated with hinge defects in D-veligers. This study shows, for the first time, that ocean acidification affects larval soft-tissue development, independent from calcification. Multiple developmental processes additively underpin the teratogenic effect of ocean acidification on bivalve larvae. These results explain why trochophores are the most sensitive life-history stage in marine bivalves and suggest that short-term variability in carbonate chemistry can impact early larval development.

OCEANOGRAPHY. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios.

The ocean moderates anthropogenic climate change at the cost of profound alterations of its physics, chemistry, ecology, and services. Here, we evaluate and compare the risks of impacts on marine and coastal ecosystems­and the goods and services they provide­for growing cumulative carbon emissions under two contrasting emissions scenarios. The current emissions trajectory would rapidly and significantly alter many ecosystems and the associated services on which humans heavily depend. A reduced emissions scenario­consistent with the Copenhagen Accord's goal of a global temperature increase of less than 2°C­is much more favorable to the ocean but still substantially alters important marine ecosystems and associated goods and services. The management options to address ocean impacts narrow as the ocean warms and acidifies. Consequently, any new climate regime that fails to minimize ocean impacts would be incomplete and inadequate.

Rapid acclimation of juvenile corals to CO2 -mediated acidification by upregulation of heat shock protein and Bcl-2 genes.

Corals play a key role in ocean ecosystems and carbonate balance, but their molecular response to ocean acidification remains unclear. The only previous whole-transcriptome study (Moya et al. Molecular Ecology, 2012; 21, 2440) documented extensive disruption of gene expression, particularly of genes encoding skeletal organic matrix proteins, in juvenile corals (Acropora millepora) after short-term (3 d) exposure to elevated pCO2 . In this study, whole-transcriptome analysis was used to compare the effects of such 'acute' (3 d) exposure to elevated pCO2 with a longer ('prolonged'; 9 d) period of exposure beginning immediately post-fertilization. Far fewer genes were differentially expressed under the 9-d treatment, and although the transcriptome data implied wholesale disruption of metabolism and calcification genes in the acute treatment experiment, expression of most genes was at control levels after prolonged treatment. There was little overlap between the genes responding to the acute and prolonged treatments, but heat shock proteins (HSPs) and heat shock factors (HSFs) were over-represented amongst the genes responding to both treatments. Amongst these was an HSP70 gene previously shown to be involved in acclimation to thermal stress in a field population of another acroporid coral. The most obvious feature of the molecular response in the 9-d treatment experiment was the upregulation of five distinct Bcl-2 family members, the majority predicted to be anti-apoptotic. This suggests that an important component of the longer term response to elevated CO2 is suppression of apoptosis. It therefore appears that juvenile A. millepora have the capacity to rapidly acclimate to elevated pCO2 , a process mediated by upregulation of specific HSPs and a suite of Bcl-2 family members.

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.

Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals.

Global environmental changes, including ocean acidification, have been identified as a major threat to scleractinian corals. General predictions are that ocean acidification will be detrimental to reef growth and that 40 to more than 80 per cent of present-day reefs will decline during the next 50 years. Cold-water corals (CWCs) are thought to be strongly affected by changes in ocean acidification owing to their distribution in deep and/or cold waters, which naturally exhibit a CaCO(3) saturation state lower than in shallow/warm waters. Calcification was measured in three species of Mediterranean cold-water scleractinian corals (Lophelia pertusa, Madrepora oculata and Desmophyllum dianthus) on-board research vessels and soon after collection. Incubations were performed in ambient sea water. The species M. oculata was additionally incubated in sea water reduced or enriched in CO(2). At ambient conditions, calcification rates ranged between -0.01 and 0.23% d(-1). Calcification rates of M. oculata under variable partial pressure of CO(2) (pCO(2)) were the same for ambient and elevated pCO(2) (404 and 867 µatm) with 0.06 ± 0.06% d(-1), while calcification was 0.12 ± 0.06% d(-1) when pCO(2) was reduced to its pre-industrial level (285 µatm). This suggests that present-day CWC calcification in the Mediterranean Sea has already drastically declined (by 50%) as a consequence of anthropogenic-induced ocean acidification.

Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris.

The anthropogenic release of carbon dioxide (CO(2)) into the atmosphere leads to an increase in the CO(2) partial pressure (pCO(2)) in the ocean, which may reach 950 µatm by the end of the 21st century. The resulting hypercapnia (high pCO(2)) and decreasing pH ("ocean acidification") are expected to have appreciable effects on water-breathing organisms, especially on their early-life stages. For organisms like squid that lay their eggs in coastal areas where the embryo and then paralarva are also exposed to metal contamination, there is a need for information on how ocean acidification may influence trace element bioaccumulation during their development. In this study, we investigated the effects of enhanced levels of pCO(2) (380, 850 and 1500 µatm corresponding to pH(T) of 8.1, 7.85 and 7.60) on the accumulation of dissolved (110m)Ag, (109)Cd, (57)Co, (203)Hg, (54)Mn and (65)Zn radiotracers in the whole egg strand and in the different compartments of the egg of Loligo vulgaris during the embryonic development and also in hatchlings during their first days of paralarval life. Retention properties of the eggshell for (110m)Ag, (203)Hg and (65)Zn were affected by the pCO(2) treatments. In the embryo, increasing seawater pCO(2) enhanced the uptake of both (110m)Ag and (65)Zn while (203)Hg showed a minimum concentration factor (CF) at the intermediate pCO(2). (65)Zn incorporation in statoliths also increased with increasing pCO(2). Conversely, uptake of (109)Cd and (54)Mn in the embryo decreased as a function of increasing pCO(2). Only the accumulation of (57)Co in embryos was not affected by increasing pCO(2). In paralarvae, the CF of (110m)Ag increased with increasing pCO(2), whereas the (57)Co CF was reduced at the highest pCO(2) and (203)Hg showed a maximal uptake rate at the intermediate pCO(2). (54)Mn and (65)Zn accumulation in paralarvae were not significantly modified by hypercapnic conditions. Our results suggest a combined effect of pH on the adsorption and protective properties of the eggshell and of hypercapnia on the metabolism of embryo and paralarvae, both causing changes to the accumulation of metals in the tissues of L. vulgaris.

Measurement of community metabolism and significance in the coral reef CO2 source-sink debate.

Two methods are commonly used to measure the community metabolism (primary production, respiration, and calcification) of shallow-water marine communities and infer air-sea CO2 fluxes: the pH-total alkalinity and pH-O2 techniques. The underlying assumptions of each technique are examined to assess the recent claim that the most widely used technique in coral reefs (pH-total alkalinity), may have provided spurious results in the past because of high rates of nitrification and release of phosphoric acid in the water column [Chisholm, J. R. M. & Barnes, D. J. (1998) Proc. Natl. Acad. Sci. USA 95, 6566-6569]. At least three lines of evidence suggest that this claim is not founded. First, the rate of nitrification required to explain the discrepancy between the two methods recently reported is not realistic as it is much higher than the rates measured in another reef system and greater than the highest rate measured in a marine environment. Second, fluxes of ammonium, nitrate, and phosphorus are not consistent with high rates of nitrification and release of phosphoric acid. Third, the consistency of the metabolic parameters obtained by using the two techniques is in good agreement in two sites recently investigated. The pH-total alkalinity technique therefore appears to be applicable in most coral reef systems. Consequently, the conclusion that most coral reef flats are sources of CO2 to the atmosphere does not need revision. Furthermore, we provide geochemical evidence that calcification in coral reefs, as well as in other calcifying ecosystems, is a long-term source of CO2 for the atmosphere.