Galápagos coral reef persistence after ENSO warming across an acidification gradient

Anthropogenic CO2 is causing warming and ocean acidification. Coral reefs are being severely impacted, yet confusion lingers regarding how reefs will respond to these stressors over this century. Since the 1982-1983 El Niño-Southern Oscillation warming event, the persistence of reefs around the Galápagos Islands has differed across an acidification gradient. Reefs disappeared where pH<8.0 and aragonite saturation state (Omega arag)<=3 and have not recovered, whereas one reef has persisted where pH>8.0 and Omega arag>3. Where upwelling is greatest, calcification by massive Porites is higher than predicted by a published relationship with temperature despite high CO2, possibly due to elevated nutrients. However, skeletal P/Ca, a proxy for phosphate exposure, negatively correlates with density (R=-0.822, p<0.0001). We propose that elevated nutrients have the potential to exacerbate acidification by depressing coral skeletal densities and further increasing bioerosion already accelerated by low pH.

Coral-algae metabolism and diurnal changes in the CO2-carbonate system of bulk sea water

Precise measurements were conducted in continuous flow seawater mesocosms located in full sunlight that compared metabolic response of coral, coral-macroalgae and macroalgae systems over a diurnal cycle. Irradiance controlled net photosynthesis (Pnet), which in turn drove net calcification (Gnet), and altered pH. Pnet exerted the dominant control on [CO3]2- and aragonite saturation state (Omega arag) over the diel cycle. Dark calcification rate decreased after sunset, reaching zero near midnight followed by an increasing rate that peaked at 03:00 h. Changes in Omega arag and pH lagged behind Gnet throughout the daily cycle by two or more hours. The flux rate Pnet was the primary driver of calcification. Daytime coral metabolism rapidly removes dissolved inorganic carbon (DIC) from the bulk seawater and photosynthesis provides the energy that drives Gnet while increasing the bulk water pH. These relationships result in a correlation between Gnet and Omega arag, with Omega arag as the dependent variable. High rates of H+ efflux continued for several hours following mid-day peak Gnet suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Hypothesis. DIC flux (uptake) followed Pnet and Gnet and dropped off rapidly following peak Pnet and peak Gnet indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H+. Over a 24 h period the plot of total alkalinity (AT) versus DIC as well as the plot of Gnet versus Omega arag revealed a circular hysteresis pattern over the diel cycle in the coral and coral-algae mesocosms, but not the macroalgae mesocosm. Presence of macroalgae did not change Gnet of the corals, but altered the relationship between Omega arag and Gnet. Predictive models of how future global changes will effect coral growth that are based on oceanic Omega arag must include the influence of future localized Pnet on Gnet and changes in rate of reef carbonate dissolution. The correlation between Omega arag and Gnet over the diel cycle is simply the response of the CO2-carbonate system to increased pH as photosynthesis shifts the equilibria and increases the [CO3]2- relative to the other DIC components of [HCO3]- and [CO2]. Therefore Omega arag closely tracked pH as an effect of changes in Pnet, which also drove changes in Gnet. Measurements of DIC flux and H+ flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.

Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions

Coral reef ecosystems develop best in high-flow environments but their fragile frameworks are also vulnerable to high wave energy. Wave-resistant algal rims, predominantly made up of the crustose coralline algae (CCA) Porolithon onkodes and P. pachydermum, are therefore critical structural elements for the survival of many shallow coral reefs. Concerns are growing about the susceptibility of CCA to ocean acidification because CCA Mg-calcite skeletons are more susceptible to dissolution under low pH conditions than coral aragonite skeletons. However, the recent discovery of dolomite (Mg0.5Ca0.5(CO3)), a stable carbonate, in P. onkodes cells necessitates a reappraisal of the impacts of ocean acidification on these CCA. Here we show, using a dissolution experiment, that dried dolomite-rich CCA have 6-10 times lower rates of dissolution than predominantly Mg-calcite CCA in both high-CO2 (~ 700 ppm) and control (~ 380 ppm) environments, respectively. We reveal this stabilizing mechanism to be a combination of reduced porosity due to dolomite infilling and selective dissolution of other carbonate minerals. Physical break-up proceeds by dissolution of Mg-calcite walls until the dolomitized cell eventually drops out intact. Dolomite-rich CCA frameworks are common in shallow coral reefs globally and our results suggest that it is likely that they will continue to provide protection and stability for coral reef frameworks as CO2 rises.

Seawater carbonate chemistry and dark respiration and photosynthetic capacity during experiments with coral Acropora formosa, 2010

Ocean acidification is expected to lower the net accretion of coral reefs yet little is known about its effect on coral photophysiology. This study investigated the effect of increasing CO2 on photosynthetic capacity and photoprotection in Acropora formosa. The photoprotective role of photorespiration within dinoflagellates (genus Symbiodinium) has largely been overlooked due to focus on the presence of a carbon-concentrating mechanism despite the evolutionary persistence of a Form II Rubisco. The photorespiratory fixation of oxygen produces phosphoglycolate that would otherwise inhibit carbon fixation though the Calvin cycle if it were not converted to glycolate by phosphoglycolate phosphatase (PGPase). Glycolate is then either excreted or dealt with by enzymes in the photorespiratory glycolate and/or glycerate pathways adding to the pool of carbon fixed in photosynthesis. We found that CO2 enrichment led to enhanced photoacclimation (increased chlorophyll a per cell) to the subsaturating light levels. Light-enhanced dark respiration per cell and xanthophyll de-epoxidation increased, with resultant decreases in photosynthetic capacity (Pnmax) per chlorophyll. The conservative CO2 emission scenario (A1B; 600-790 ppm) led to a 38% increase in the Pnmax per cell whereas the 'business-as-usual' scenario (A1F1; 1160-1500 ppm) led to a 45% reduction in PGPase expression and no change in Pnmax per cell. These findings support an important functional role for PGPase in dinoflagellates that is potentially compromised under CO2 enrichment.

Seawater carbonate chemistry and biological processes of coral Acropora muricata during experiments and observations in La Saline fringing reef, La Reunion Island, western Indian Ocean, 2011

The effect of decreasing aragonite saturation state (Omega Arag) of seawater (elevated pCO2) on calcification rates of Acropora muricata was studied using nubbins prepared from parent colonies located at two sites of La Saline reef (La Réunion Island, western Indian Ocean): a back-reef site (BR) affected by nutrient-enriched groundwater discharge (mainly nitrate), and a reef flat site (RF) with low terrigenous inputs. Protein and chlorophyll a content of the nubbins, as well as zooxanthellae abundance, were lower at RF than BR. Nubbins were incubated at ~27°C over 2 h under sunlight, in filtered seawater manipulated to get differing initial pCO2 (1,440-340 µatm), Omega Arag (1.4-4.0), and dissolved inorganic carbon (DIC) concentrations (2,100-1,850 µmol/kg). Increasing DIC concentrations at constant total alkalinity (AT) resulted in a decrease in Omega Arag and an increase in pCO2. AT at the beginning of the incubations was kept at a natural level of 2,193 ± 6 µmol/kg (mean ± SD). Net photosynthesis (NP) and calcification were calculated from changes in pH and AT during the incubations. Calcification decrease in response to doubling pCO2 relative to preindustrial level was 22% for RF nubbins. When normalized to surface area of the nubbins, (1) NP and calcification were higher at BR than RF, (2) NP increased in high pCO2 treatments at BR compared to low pCO2 treatments, and (3) calcification was not related to Omega Arag at BR. When normalized to NP, calcification was linearly related to Omega Arag at both sites, and the slopes of the relationships were not significantly different. The increase in NP at BR in the high pCO2 treatments may have increased calcification and thus masked the negative effect of low Omega Arag on calcification. Removing the effect of NP variations at BR showed that calcification declined in a similar manner with decreased Omega Arag (increased pCO2) whatever the nutrient loading.

Growth, respiration and photophysiology of coral massive Porites spp. in the experiment of Moorea

I tested the hypothesis that high pCO2 (76.6 Pa and 87.2 Pa vs. 42.9 Pa) has no effect on the metabolism of juvenile massive Porites spp. after 11 days at 28 °C and 545 µmol quanta/m**2/s. The response was assessed as aerobic dark respiration, skeletal weight (i.e., calcification), biomass, and chlorophyll fluorescence. Corals were collected from the shallow (3-4 m) back reef of Moorea, French Polynesia (17°28.614'S, 149°48.917'W), and experiments conducted during April and May 2011. An increase in pCO2 to 76.6 Pa had no effect on any dependent variable, but 87.2 Pa pCO2 reduced area-normalized (but not biomass-normalized) respiration 36 %, as well as maximum photochemical efficiency (Fv/Fm) of open RCIIs and effective photochemical efficiency of RCIIs in actinic light (Delta F/F'm ); neither biomass, calcification, nor the energy expenditure coincident with calcification (J/g) was effected. These results do not support the hypothesis that high pCO2 reduces coral calcification through increased metabolic costs and, instead, suggest that high pCO2 causes metabolic depression and photochemical impairment similar to that associated with bleaching. Evidence of a pCO2 threshold between 76.6 and 87.2 Pa for inhibitory effects on respiration and photochemistry deserves further attention as it might signal the presence of unpredictable effects of rising pCO2.

Seawater carbonate chemistry and calcification during a study of barrier reef flat in Moorea, French Polynesia, 1998

The relative contribution of soft bottoms to the community metabolism (primary production, respiration and net calcification) of a barrier reef flat has been investigated at Moorea (French Polynesia). Community metabolism of the sedimentary area was estimated using in situ incubations in perspex chambers, and compared with estimates of community metabolism of the whole reef flat obtained using a Lagrangian technique (Gattuso et al., 1996. Carbon flux in coral reefs. 1. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar. Ecol. Prog. Ser. 145, 109-121). Net organic carbon production (E), respiration (R) and net calcification (G) of sediments were measured by seven incubations performed in triplicate at different irradiance. Respiration and environmental parameters were also measured at four randomly selected additional stations. A model of Photosynthesis-irradiance allowed to calculate oxygen (O2), organic carbon (CO2) and calcium carbonate (CaCO3) evolution from surface irradiance during a diel cycle. As chlorophyll a content of the sediment was not significantly different between stations, primary production of the sediment was considered as homogeneous for the whole lagoon. Thus, carbon production at the test station can be modelled from surface light irradiance. The modelled respiration was two times higher at the test station than the mean respiration of the barrier reef, and thus underestimated sediment contribution to excess production. Sediments cover 40-60% of the surface and accounted for 2.8-4.1% of organic carbon excess production estimated with the modelled R and 21-32% when mean R value was considered. The sedimentary CaCO3 budget was a very minor component of the whole reef budget.

Rates of nitrogen cycling and chemo-autotrophy in the cold-water coral Lophelia pertusa

Cold-water corals (CWC) are widely distributed around the world forming extensive reefs at par with tropical coral reefs. They are hotspots of biodiversity and organic matter processing in the world's deep oceans. Living in the dark they lack photosynthetic symbionts and are therefore considered to depend entirely on the limited flux of organic resources from the surface ocean. While symbiotic relations in tropical corals are known to be key to their survival in oligotrophic conditions, the full metabolic capacity of CWC has yet to be revealed. Here we report isotope tracer evidence for efficient nitrogen recycling, including nitrogen assimilation, regeneration, nitrification and denitrification. Moreover, we also discovered chemoautotrophy and nitrogen fixation in CWC and transfer of fixed nitrogen and inorganic carbon into bulk coral tissue and tissue compounds (fatty acids and amino acids). This unrecognized yet versatile metabolic machinery of CWC conserves precious limiting resources and provides access to new nitrogen and organic carbon resources that may be essential for CWC to survive in the resource-depleted dark ocean.