Spatial competition dynamics between reef corals under ocean acidification

Climate change, including ocean acidification (OA), represents a major threat to coral-reef ecosystems. Although previous experiments have shown that OA can negatively affect the fitness of reef corals, these have not included the long-term effects of competition for space on coral growth rates. Our multispecies year-long study subjected reef-building corals from the Gulf of Aqaba (Red Sea) to competitive interactions under present-day ocean pH (pH 8.1) and predicted end-of-century ocean pH (pH 7.6). Results showed coral growth is significantly impeded by OA under intraspecific competition for five out of six study species. Reduced growth from OA, however, is negligible when growth is already suppressed in the presence of interspecific competition. Using a spatial competition model, our analysis indicates shifts in the competitive hierarchy and a decrease in overall coral cover under lowered pH. Collectively, our case study demonstrates how modified competitive performance under increasing OA will in all likelihood change the composition, structure and functionality of reef coral communities

Impact of ocean acidification on crystallographic vital effect of the coral skeleton

Distinguishing between environmental and species-specific physiological signals, recorded in coral skeletons, is one of the fundamental challenges in their reliable use as (paleo)climate proxies. To date, characteristic biological bias in skeleton-recorded environmental signatures (vital effect) was shown in shifts in geochemical signatures. Herein, for the first time, we have assessed crystallographic parameters of bio-aragonite to study the response of the reefbuilding coral Stylophora pistillata to experimental seawater acidification (pH 8.2, 7.6 and 7.3). Skeletons formed under high pCO2 conditions show systematic crystallographic changes such as better constrained crystal orientation and anisotropic distortions of bio-aragonite lattice parameters due to increased amount of intracrystalline organic matrix and water content. These variations in crystallographic features that seem to reflect physiological adjustments of biomineralizing organisms to environmental change, are herein called crystallographic vital effect (CVE). CVE may register those changes in the biomineralization process that may not yet be perceived at the macromorphological skeletal level. https://doi.org/10.1038/s41467-019-10833-6 OPEN

Measuring coral calcification under ocean acidification: methodological considerations for the 45Ca-uptake and total alkalinity anomaly technique

As the oceans become less alkaline due to rising CO2 levels, deleterious consequences are expected for calcifying corals. Predicting how coral calcification will be affected by on-going ocean acidification (OA) requires an accurate assessment of CaCO3 deposition and an understanding of the relative importance that decreasing calcification and/or increasing dissolution play for the overall calcification budget of individual corals. Here, we assessed the compatibility of the 45Ca-uptake and total alkalinity (TA) anomaly techniques as measures of gross and net calcification (GC, NC), respectively, to determine coral calcification at pHT 8.1 and 7.5. Considering the differing buffering capacity of seawater at both pH values, we were also interested in how strongly coral calcification alters the seawater carbonate chemistry under prolonged incubation in sealed chambers, potentially interfering with physiological functioning. Our data indicate that NC estimates by TA are erroneously ∼5% and ∼21% higher than GC estimates from 45Ca for ambient and reduced pH, respectively. Considering also previous data, we show that the consistent discrepancy between both techniques across studies is not constant, but largely depends on the absolute value of CaCO3 deposition. Deriving rates of coral dissolution from the difference between NC and GC was not possible and we advocate a more direct approach for the future by simultaneously measuring skeletal calcium influx and efflux. Substantial changes in carbonate system parameters for incubation times beyond two hours in our experiment demonstrate the necessity to test and optimize experimental incubation setups when measuring coral calcification in closed systems, especially under OA conditions

Symbiosis-specific changes in dimethylsulphoniopropionate concentrations in Stylophora pistillata along a depth gradient

Scleractinian corals are prolific producers of dimethylsulphoniopropionate (DMSP), but ecophysiological mechanisms influencing cellular concentrations are uncertain. While DMSP is often proposed to function as an antioxidant, interactions between specific host–symbiont genotype associations, plasticity in DMSP concentrations and environmental conditions that can either exert or alleviate oxidative stress are unclear. We used long-term (6 months) reciprocal transplantation of Stylophora pistillata hosting two distinct symbiont phylotypes along a depth gradient, clades A (20 m), to assess the effect of change in depth (light intensity) on DMSP concentrations in relation to symbiont genotype and photoacclimation in corals between 3 and 50 m in the Gulf of Aqaba. Bathymetric distribution of total DMSP (DMSPt) per cell varied significantly while particulate DMSP (DMSPp) appeared to be unaffected by depth. Highest DMSPt concentrations in control corals occurred at 20 m. While 3-m transplants showed a significant increase in DMSPt concentration at 20 m and became affiliated with an additional genotype (C72), 50-m transplants largely persisted with their original genotype and exhibited no significant changes in DMSPt concentrations. DMSPt concentrations in transplants at both 3 and 50 m, on the other hand, increased significantly while all corals maintained their original symbiont genotypes. Photoacclimation differed significantly with transplantation direction relative to the controls. Symbionts in 3-m transplants at 20 m exhibited no changes in chlorophyll a (chl a) concentration, cell density or cell diameter while symbiont densities decreased and chl a concentrations increased significantly at 50 m. In contrast, symbiont densities in 50-m transplants remained unaffected across depths while symbiont diameters decreased. Chl a concentrations decreased at 20 m and increased at 3 m. Our results indicate that DMSPt concentrations following changes in depth are not only a function of symbiont genotype but result from different acclimation abilities of both symbiotic partners

Coral bleaching following wintry weather

Extensive coral bleaching Occurred intertidally in early August 2003 in the Capricorn Bunker group (Wistari Reef, Heron and One Tree Islands; Southern Great Barrier Reef). The affected intertidal coral had been exposed to unusually cold (minimum = 13.3degreesC; wet bulb temperature = 9degreesC) and dry winds (44% relative humidity) for 2 d during predawn low tides. Coral bleached in the upper 10 cm of their branches and had less than 0.2 x 10(6) cell cm(-2) as compared with over 2.5 x 10(6), Cell cm(-2) in nonbleached areas. Dark-adapted quantum yields did not differ between symbionts in bleached and nonbleached areas. Exposing symbionts to light, however, led to greater quenching of Photosystem 11 in symbionts in the bleached coral. Bleached areas of the affected colonies had died by September 2003, with areas that were essentially covered by more than 80% living coral decreasing to less than 10% visible living coral cover. By January 2004, coral began to recover, principally from areas of colonies that were not exposed during low tide (i.e., from below dead, upper regions). These data highlight the importance of understanding local weather patterns as well as the effects of longer term trends in global climate

Coral photosymbiosis: Linking phylogenetic identity to single cell metabolic activity in mixed symbiont populations

Tropical reef-building corals live in symbiosis with a wide range of micro-organisms, including unicellular Symbiodinium dinoflagellates also called zooxanthellae. These photosynthetic endosymbionts live inside the coral gastroderm cells. Although corals can feed on planktonic preys, the dinoflagellates significantly contribute to the nutrition of their host by transferring a large fraction (up to 90%) of photosynthates that are produced through the fixation of dissolved inorganic carbon (DIC) and nitrogen (nitrate or ammonium). Nine major clades (A-I) of Symbiodinium have been identified by molecular genetic analyses. Each clade presents distinct physiological features and the specific association between coral species and Symbiodinium clade determines the phenotype of the holobiont. Differences in the photosynthetic response to irradiance, rates of carbon fixation, and thermal tolerance can be attributed to symbiont clade. Several Symbiodinium clades can simultaneously exist within a single coral and the host can dynamically modify the proportion between dominant and background clades to adapt to changing environmental conditions. Investigating at the cellular level the metabolic exchanges between coral and Symbiodinium is of great interest to understand e.g. the bleaching process (loss of zooxanthellae) which often leads to coral death. We are aiming at quantitatively image the differential metabolic activity between symbiont clades in the same host, in the intact symbiosis. Previous studies have used mass bulk techniques to investigate the metabolism of symbionts at the colony scale. However, such studies cannot determine the specific contribution of the individual cells, as a function of their distribution in the coral host tissue. We have developed a SIMS-ISH method combining nanoscale secondary ion mass spectrometry (NanoSIMS) and in situ hybridization (ISH) for the simultaneous in situ identification of Symbiodinium genotype, and visualization of symbiont-host metabolic exchange at the level of individual cell. We focus on two reef-building coral species Pocillopora damicornis and Stylophora pistillata for which a large amount of complementary metabolic data exists. We designed specific fluorescent DNA probes to identify clade C Symbiodinium in P. damicornis and clade A in S. pistillata, and in mixed cultures. We combined the probes with pulse-chase experiments using isotopically labeled seawater (13C-bicarbonate and 15N-nitrate) to attribute a particular metabolism to a specific clade. This combined method enables us to phylogenetically identify metabolically active cells from a NanoSIMS isotopic/elemental image. The precise correlation between TEM and the NanoSIMS isotopic maps allows us to follow the turnover and translocation of metabolites with sub-cellular precision in both the symbionts and the host. Due to the complex nature of the coral symbiosis, the ability to discriminate the phylogenetic identity and metabolic role of specific Symbiodinium populations in situ is crucial to understand the effects of environmental stress on the coral holobiont plasticity. Moreover, analyzing symbiotic associations in situ provides a unique insight into the spatio-temporal patterns of metabolic interactions in holobionts. This analytical breakthrough promises to open entirely new areas of research focused on understanding the dynamics of interactions between animals and the microbial world

Light from down under

Coral-algae symbiosis is a key feature of tropical corals and is highly dependent on the efficiency with which solar energy is attenuated by the coral. Scleractinian corals are among the most efficient light collectors in nature because of the modulation of the internal light field in the coral skeleton. Interestingly, coral skeleton particles composing the sandy bottoms in reef margins sustain these optical characteristics. In the present study, we examined two free-living coral species - Heterocyathus aequicostatus (Caryophyllidae) and Heteropsammia cochlea (Dendrophylliidae) - common on biogenic coarse carbonate sand of the Great Barrier Reef but absent from fine sand at the same depth. In coarse carbonate sand, light penetrates a few millimeters below the surface and propagates along horizontal distances of a few centimeters. In fine sand, almost all of the light is reflected back to the water column. For photosynthetic sand-dwelling organisms such as the studied species, with over one-third of their surface area facing the substrate, light flux to their underside may be beneficial. A correlation was found between the diameter of these corals and the distance that light may travel in the sand under the coral. Laboratory and field measurements show that the symbiotic algae on the underside of the corallites are photosynthetically active even when the coral is partially buried, implying sufficient light penetration. Other organisms in the study site, such as fungid corals and foraminiferans, with different morphologies, have different light-trapping strategies but are also photosynthesizing on their underside. The importance of the substrate type to the performance of the three main partners of the symbiosis (coral, endosymbiotic algae and a sipunculan worm) is highlighted, and is a striking example of co-evolution

Assessment of Temperature Optimum Signatures of Corals at Both Latitudinal Extremes of the Red Sea

Rising ocean temperatures are pushing reef-building corals beyond their temperature optima (Topt), resulting in reduced physiological performances and increased risk of bleaching. Identifying refugia with thermally resistant corals and understanding their thermal adaptation strategy is therefore urgent to guide conservation actions. The Gulf of Aqaba (GoA, northern Red Sea) is considered a climate refuge, hosting corals that may originate from populations selected for thermal resistance in the warmer waters of the Gulf of Tadjoura (GoT, entrance to the Red Sea and 2000 km south of the GoA). To better understand the thermal adaptation strategy of GoA corals, we compared the temperature optima (Topt) of six common reef-building coral species from the GoA and the GoT by measuring oxygen production and consumption rates as well as photophysiological performance (i.e. chlorophyll fluorescence) in response to a short heat stress. Most species displayed similar Topt between the two locations, highlighting an exceptional continuity in their respective physiological performances across such a large latitudinal range, supporting the GoA refuge theory. Stylophora pistillata showed a significantly lower Topt in the GoA, which may suggest an ongoing population-level selection (i.e. adaptation) to the cooler waters of the GoA and subsequent loss of thermal resistance. Interestingly, all Topt were significantly above the local maximum monthly mean seawater temperatures in the GoA (27.1°C) and close or below in the GoT (30.9°C), indicating that GoA corals, unlike those in the GoT, may survive ocean warming in the next few decades. Finally, Acropora muricata and Porites lobata displayed higher photophysiological performance than most species, which may translate to dominance in local reef communities under future thermal scenarios. Overall, this study is the first to compare the Topt of common reef-building coral species over such a latitudinal range and provides insights into their thermal adaptation in the Red Sea

A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

Abstract: A wide range of organisms host photosynthesizing symbionts. In these animals the metabolic exchange between host and symbionts has prevented in situ host anabolic turnover to be studied without the confounding effect of translocated photosynthates. Using the symbiotic coral Stylophora pistillata as a model organism and [1-13C]-pyruvate and [2,3-13C]-pyruvate in different incubation conditions (light, light + DCMU, and darkness), we employed NanoSIMS isotopic imaging to quantify host anabolism, with and without translocated metabolites from their photosynthesizing dinoflagellate symbionts. Under our experimental conditions, host de novo lipid synthesis accounted for ~40% of the total holobiont lipid reserve, and dinoflagellate recycling of metabolic 13CO2 enhanced host tissue 13C-enrichment by 13–22% in the epidermis, 40–58% in the gastrodermis, and 135–169% in host lipid bodies. Furthermore, we show that host anabolic turnover in different tissue structures differs, in a manner consistent with the localisation, function and cellular composition of these structures

A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

Abstract: A wide range of organisms host photosynthesizing symbionts. In these animals the metabolic exchange between host and symbionts has prevented in situ host anabolic turnover to be studied without the confounding effect of translocated photosynthates. Using the symbiotic coral Stylophora pistillata as a model organism and [1-13C]-pyruvate and [2,3-13C]-pyruvate in different incubation conditions (light, light + DCMU, and darkness), we employed NanoSIMS isotopic imaging to quantify host anabolism, with and without translocated metabolites from their photosynthesizing dinoflagellate symbionts. Under our experimental conditions, host de novo lipid synthesis accounted for ~40% of the total holobiont lipid reserve, and dinoflagellate recycling of metabolic 13CO2 enhanced host tissue 13C-enrichment by 13–22% in the epidermis, 40–58% in the gastrodermis, and 135–169% in host lipid bodies. Furthermore, we show that host anabolic turnover in different tissue structures differs, in a manner consistent with the localisation, function and cellular composition of these structures