Skeletal δ13C Research Articles

Variability of skeletal growth and δ13C in massive corals from the South China Sea: Effects of photosynthesis, respiration and human activities

The δ 13C, skeletal density and extension rates were analyzed along same growth axes of massive coral colonies collected from the shallow sea to the east and south of Hainan Island, northern South China Sea. Seasonal changes of δ 13C, extension and calcification rates of Porites lutea and Porites lobata are in phase and correlated with solar radiation. In addition, annual high δ 13C values, extension and calcification rates occur in spring and low values and rates occur in late autumn or early winter. The annual highest density band of P. lutea formed in spring and the lowest ones in early winter, whereas P. lobata shows only a weak seasonal density change. We suggest that the seasonal features of the coral δ 13C, extension and calcification rates are modulated by light-induced photosynthesis determined by solar radiation reaching the top of the atmosphere, and by cloud coverage. The results also support the suggestion that photosynthesis promotes both the extension growth and skeleton thickening for P. lutea, but that it mainly promotes the extension growth for P. lobata. Remarkable inter-decadal trends are evident in the coral records; these trends are progressive decreases of skeletal δ 13C, density and calcification rate, and an increase of the extension rate over the last 30 years, which are marked by abrupt changes at about 1987. These trends are ascribed to intensified coral respiration arising from rising temperature, together with the effects of declining nutrient levels caused by the destruction of the coastal ecosystem in the sampling regions.

Effect of photosynthetic light dosage on carbon isotope composition in the coral skeleton: Long‐term culture of Porites spp.

Whereas the oxygen isotope ratio of the coral skeleton is used for reconstruction of past information on seawater, the carbon isotope ratio is considered a proxy for physiological processes, principally photosynthesis and respiration. However, the fractionation of carbon isotopes in biogenic carbonate such as coral skeleton is still unclear. We conducted a long‐term culture experiment of Porites spp. corals at different light dosages (light intensity, 100, 300, or 500 μmol m−2 s−1; daily light period, 10 or 12 h) at 25 ± 0.6°C to examine the contribution of photosynthetic activity to skeletal carbon isotope composition. Corals were grown in sand‐filtered seawater and not fed; thus, they subsisted from photosynthesis of symbiotic algae. As the daily dose of photosynthetically active radiation increased, the rate of annual extension also increased. Mean isotope compositions shifted; the carbon isotope compositions (δ13C) became heavier and the oxygen isotope compositions (δ18O) became lighter at higher radiation dose. Skeletal δ18O decrease coincided with increasing skeletal growth rate, indicating the influence of so‐called kinetic isotope effects. The observed δ13C increase should be subject to both kinetic and metabolic isotope effects, with the latter reflecting skeletal δ13C enrichment due to photosynthesis by symbiotic algae. Using a vector approach in the δ13C–δ18O plane, we discriminated between kinetic and metabolic isotope effects on δ13C. The calculated δ13C changes from metabolic isotope effects were light dose dependent. The δ13C fractionation curve related to metabolic isotope effects is very similar to the photosynthesis–irradiance curve, indicating the direct contribution of photosynthetic activity to metabolic isotope effects. In contrast, δ13C fractionation related to kinetic isotope effects gradually increased as the growth rate increased. Our experiment demonstrated that the kinetic and metabolic isotope effects in coral skeleton were successfully differentiated.

Impact of skeletal dissolution and secondary aragonite on trace element and isotopic climate proxies in Porites corals

Restricted zones of recent dissolution and secondary aragonite infilling were identified in a coral core collected in 1986 from a living massive Porites colony from the central Great Barrier Reef, Australia. Secondary aragonite needles, ≥20 μm long, cover skeletal surfaces deposited from 1972 to late 1974 and increase bulk density by 10%. Dissolution is observed above this zone, whereas older skeleton is pristine. We investigate the impact of both types of early marine diagenesis on skeletal geochemistry and coral paleoclimate reconstructions by comparison with similar records from eight contemporary Porites colonies collected at nearby reefs. Secondary aragonite overgrowth causes anomalies in skeletal density, Mg/Ca, Sr/Ca, U/Ca, δ18O, and δ13C. The secondary aragonite is consistently associated with a cool temperature anomaly for each of the sea surface temperature (SST) proxies (δ18O‐SST −1.6°C; Sr/Ca‐SST −1.7°C; Mg/Ca‐SST −1.9°C; U/Ca‐SST −2.8°C). Dissolution, through incongruent leaching, also causes cool SST artifacts but only for trace element ratios (Mg/Ca‐SST −1.2°C; Sr/Ca‐SST −1.2°C; U/Ca‐SST −2.1°C). The sequence of preference with respect to dissolution of coral skeleton in seawater is Mg > Ca > Sr > U. Rigorous screening of coral material for paleoclimate reconstructions is therefore necessary to detect both dissolution and the presence of secondary minerals. The excellent agreement between apparent SST anomalies generated by different modes of diagenesis means that replication of tracers within a single coral cannot be used to validate climate‐proxy interpretations. Poor replication of records between different coral colonies, however, provides a strong indication of nonclimatic artifacts such as dissolution and secondary aragonite.

Pre-treatment effects on coral skeletal δ13C and δ18O

Pre-treatments are often used to remove organic “contaminant” material prior to isotopic analyses of coral skeletal samples. Here we conducted three experiments to test the pre-treatment effect of water, 30% hydrogen peroxide (H 2O 2), and household bleach [5.25% sodium hypochlorite (NaClO 3) and 0.15% sodium hydroxide (NaOH)], on the stable isotopic composition of coral skeletal samples. First, using a mass balance approach we calculated the expected change in skeletal δ 13C due to the removal of all organic carbon. The model showed that (1) the removal of organic carbon (which has a low δ 13C value relative to skeletal δ 13C) from the skeletal sample should theoretically result in a higher δ 13C value of the remaining organic-carbon-free carbonate, and that (2) only at the highest concentrations of skeletal organic carbon within the tissue layer of corals is the contribution of the organic carbon to the overall δ 13C skeletal value potentially large enough to be detectable by mass spectrometry. We then conducted two sets of experiments to test the model where we pre-treated a large number of skeletal samples from five species of corals with water, H 2O 2, bleach, or no pre-treatment for 24 h. Skeletal δ 13C generally decreased significantly with water, bleach, and H 2O 2 pre-treatments which is contrary to the model-predicted increase in δ 13C following such pre-treatments. Thus, organic carbon within the skeleton is not a net source of contamination to δ 13C analyses. Skeletal δ 18O decreased the most with water and bleach pre-treatments. In addition, the effect of H 2O 2 or bleach pre-treatments on either δ 13C or δ 18O was not consistent among species or locations. The direction of change in δ 13C and δ 18O with pre-treatments was no different for skeletal samples taken within or below the tissue layer. Based on our results, we suggest that pre-treatment is not necessary and recommend that pre-treatment not be performed on coral skeletal samples prior to stable isotope analysis to avoid any pre-treatment-induced variability that could significantly compromise inter-colony and inter-species comparisons.

Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event

Mass coral bleaching events have occurred on a global scale throughout the world’s tropical oceans and can result in large-scale coral mortality and degradation of coral reef communities. Coral bleaching has often been attributed to periods of above normal seawater temperatures and/or calm conditions with high levels of ultraviolet radiation. Unusually high shallow-water temperature (>29°C) in Kaneohe Bay, Hawaii, USA, in late summer (20 August–9 September) and fall (1–7 October) of 1996 produced visible bleaching of two dominant corals, Porites compressa Dana, 1864 and Montipora verrucosa Dana, 1864. The present study examined chlorophyll a (chl a), total lipid concentrations, and lipid class composition in corals of both species in which the entire colony was non-bleached, moderately bleached, or bleached. Skeletal, host tissue, and algal symbiont δ13C values were also measured in non-bleached and bleached colonies. In additional unevenly bleached colonies, paired samples were collected from bleached upper surfaces and non-bleached sides. Samples were collected on 20 November 1996 during the coral recovery phase, a time when seawater temperatures had been back to normal for over a month. Chl a levels were significantly lower in bleached colonies of both species compared with non-bleached specimens, and in bleached areas of unevenly bleached single colonies. Total lipid concentrations were significantly lower in bleached P. compressa compared with non-bleached colonies, whereas total lipid concentrations were the same in bleached and non-bleached M. verrucosa colonies. The proportion of triacylglycerols and wax esters was lower in bleached colonies of both species. Both bleached and non-bleached M. verrucosa had from ~17% to 35% of their lipids in the form of diacylglycerol, while this class was absent in P. compressa. δ13C was not significantly different in the host tissue and algal symbiont fractions in non-bleached and bleached samples of either species. This suggests that the ratio of carbon acquired heterotrophically versus photosynthetically was the same regardless of condition. Skeletal δ13C was significantly lower in bleached than in non-bleached corals. This is consistent with previous findings that lower rates of photosynthesis during bleaching results in lower skeletal δ13C values. The two species in this study displayed different lipid class compositions and total lipid depletions following bleaching, suggesting that there is a difference in their metabolism of lipid reserves and/or in their temporal responses to bleaching and recovery.

Effect of early marine diagenesis on coral reconstructions of surface‐ocean 13C/12C and carbonate saturation state

Recent research suggests that future decreases in the carbonate saturation state of surface seawater associated with the projected build‐up of atmospheric CO2 could cause a global decline in coral reef‐building capacity. Whether significant reductions in coral calcification are underway is a matter of considerable debate. Multicentury records of skeletal calcification extracted from massive corals have the potential to reconstruct the progressive effect of anthropogenic changes in carbonate saturation on coral reefs. However, early marine aragonite cements are commonly precipitated from pore waters in the basal portions of massive coral skeletons and, if undetected, could result in apparent nonlinear reductions in coral calcification toward the present. To address this issue, we present records of coral skeletal density, extension rate, calcification rate, δ13C, and δ18O for well preserved and diagenetically altered coral cores spanning ∼1830–1994 A.D. at Ningaloo Reef Marine Park, Western Australia. The record for the pristine coral shows no significant decrease in skeletal density or δ13C indicative of anthropogenic changes in carbonate saturation state or δ13C of surface seawater (oceanic Suess effect). In contrast, progressive addition of early marine inorganic aragonite toward the base of the altered coral produces an apparent ∼25% decrease in skeletal density toward the present, which misleadingly matches the nonlinear twentieth century decrease in coral calcification predicted by recent modeling and experimental studies. In addition, the diagenetic aragonite is enriched in 13C, relative to coral aragonite, resulting in a nonlinear decrease in δ13C toward the present that mimics the decrease in δ13C expected from the oceanic Suess effect. Taken together, these diagenetic changes in skeletal density and δ13C could be misinterpreted to reflect changes in surface‐ocean carbonate saturation state driven by the twentieth century build‐up of atmospheric CO2.

Skeletal isotope microprofiles of growth perturbations in Porites corals during the 1997?1998 mass bleaching event

Severe coral bleaching occurred throughout the tropics in 1997/98. We report high-resolution skeletal oxygen isotope (δ18O) and carbon isotope (δ13C) microprofiles for bleached corals from Pandora Reef, Great Barrier Reef, and Ishigaki Island, Japan, in order to examine the ability of Porites corals to record clear signals of bleaching. Analysis of the annual cycle in δ18O revealed abrupt reductions in skeletal extension immediately after the 1997–98 summer temperature maximum, indicating that bleaching inhibits coral calcification. Skeletal δ13C in the Ishigaki corals showed lower values during bleaching, indicating depressed coral metabolism associated with a reduction in calcification. In contrast, microprofiles of skeletal δ13C from the shaded sides of Pandora Reef corals exhibited little change, possibly because algal photosynthesis was already slow prior to bleaching, thus subduing the 13C-response to bleaching. Comparison of δ18O microprofiles from bleached corals with instrumental temperature records showed that Porites corals can recover following 5 months with little skeletogenesis. The results indicate that isotopic microprofiling may be the key to identifying gaps in coral growth that are diagnostic of past bleaching events. We have tested this hypothesis using blue UV fluorescent bands to guide us to coral skeleton where isotope microprofiling identifies bleaching events in 1986, 1989, and 1990. These events, detected by proxy, suggest that coral bleaching may have occurred more commonly on Ishigaki Island than previously recorded.

The skeletal isotopic composition as an indicator of ecological and physiological plasticity in the coral genus Madracis

Three species of the reef coral genus Madracis display skeletal isotopic characteristics that relate to depth, colony topography, and consequently to coral physiology. The joint interpretation of skeletal δ13C and δ18O provides information on the ecological plasticity and adaptation to depth of a coral species. Isotopic results are most easily understood in terms of “kinetic” effects, which reduce both δ18O and δ13C below isotopic equilibrium values, and “metabolic” effects, which only influence the skeletal δ13C. Madracis mirabilis is adapted to depths shallower than 20 m, and shows the greatest range in kinetic effects and the strongest metabolic 13C enrichments caused by symbiont photosynthesis. Madracis formosa lives deeper than 40 m, and shows a reduced range of kinetic effects and relatively weak metabolic 13C enrichments. Madracis pharensis inhabits depths from 5 to >60 m, and does not attain the strength of kinetic effects of either of the other two species, apparently because it is not quite as well adapted to rapid growth at either extreme.

Effect of light and brine shrimp on skeletal δ13C in the Hawaiian coral Porites compressa: a tank experiment

Previous experimental fieldwork showed that coral skeletal δ13C values decreased when solar intensity was reduced, and increased in the absence of zooplankton. However, actual seasonal changes in solar irradiance levels are typically less pronounced than those used in the previous experiment and the effect of increases in the consumption of zooplankton in the coral diet on skeletal δ13C remains relatively unknown. In the present study, the effects of four different light and heterotrophy regimes on coral skeletal δ13C values were measured. Porites compressa corals were grown in outdoor flow-through tanks under 112%, 100%, 75%, and 50% light conditions at the Hawaii Institute of Marine Biology, Hawaii. In addition, corals were fed either zero, low, medium, or high concentrations of brine shrimp. Decreases in light from 100% resulted in significant decreases in δ13C that is most likely due to a corresponding decrease in photosynthesis. Increases in light to 112% also resulted in a decrease in δ13C values. This latter response may be a consequence of photoinhibition. The overall curved response in δ13C values was described by a significant quadratic function. Increases in brine shrimp concentrations resulted in increased skeletal δ13C levels. This unexpected outcome appears to be attributable to enhanced nitrogen supply associated with the brine shrimp diet which led to increased zooxanthellae concentrations, increased photosynthesis rates, and thus increased δ13C values. This result highlights the potential influence of nutrients from heterotrophically acquired carbon in maintaining the zooxanthellae-host symbiosis in balance. In addition, evidence is presented that suggests that coral skeletal growth and δ13C are decoupled. These results increase our knowledge of how light and heterotrophy affects the δ13C of coral skeletons.

Isotopic partitioning between scallop shell calcite and seawater: effect of shell growth rate

The relationship between molluscan shell growth rate and skeletal δ18O and δ13C was investigated in a detailed field study for the scallop, Pecten maximus. Seasonal variation in shell growth rate was found to be a governing factor influencing shell δ18O and δ13C. At low shell growth rates, shell δ18O were more positive (of the order +0.4‰) and δ13C more negative (up to −2‰) as compared with predicted values for precipitation of inorganic calcite in isotopic equilibrium with seawater. The deviations in δ18O were hypothesized as reflecting possible differences in solution carbonate chemistry at the site of mineralization in the extrapallial fluid as compared with that of the external seawater medium. The deviations in shell δ13C were consistent with incorporation of isotopically depleted respiratory 13C (i.e., a metabolic effect). A trend toward more depleted shell δ18O and δ13C values occurred at higher shell growth rates, with negative δ18O values as compared with predicted equilibrium at shell growth rates above 0.13 mm per day. These simultaneous negative deviations in skeletal δ18O and δ13C were interpreted as resulting from a kinetic effect. The implications for environmental reconstruction from molluscan isotopic records are discussed in light of a model of isotopic behavior based on the findings of the study.

Effect of light and zooplankton on skeletal δ 13 C values in the eastern Pacific corals Pavona clavus and Pavona gigantea

Skeletal δ13C levels in symbiotic reef corals are believed to be predominantly influenced by metabolic fractionation. Therefore, environmental variables influencing coral metabolism should also affect skeletal δ13C levels. To test this hypothesis, we measured the effects of light (which drives photosynthesis) and relative zooplankton levels (heterotrophy) on skeletal δ13C values in the corals Pavona clavus and P. gigantea at two depths (1 m and 7 m). For both species, decreases in light or increases in zooplankton resulted in significant decreases in skeletal δ13C levels. A significant decrease in δ13C values with depth was observed in Pavona gigantea only. Thus, light and zooplankton directly affect coral skeletal δ13C values, supporting the hypothesis that metabolic fractionation significantly contributes to skeletal δ13C levels. Simultaneous decreases in both light and zooplankton resulted in decreases in skeletal δ13C values, reflecting decreases in light. In Pavona clavus, intra-annual variation in skeletal δ13C values over one year correlated with seasonal changes in irradiance. Further study is needed to resolve how skeletal δ13C values vary at intermediate levels of irradiance and zooplankton, and in other coral species.

Factors influencing the stable carbon and oxygen isotopic composition ofPorites lutea coral skeletons from Phuket, South Thailand

We determined the δ18O and δ13C composition of the same fixed growth increment in severalPorites lutea coral skeletons from Phuket, South Thailand. Skeletal growth rate and δ18O are inversely related. We explain this in terms of McConnaughey's kinetic isotopic disequilibria model. Annual trends in δ18O cannot be solely explained by observed variations in seawater temperature or salinity and may also reflect seasonal variations in calcification rate. Coral tissue chlorophylla content and δ13C of the underlying 1 mm of skeleton are positively related, suggesting that algal modification of the dissolved inorganic carbonate pool is the main control on skeletal δ13C. However, in corals that bleached during a period of exceptionally high seawater temperatures in the summer of 1991, δ13C of the outer 1 mm of skeleton and skeletal growth rate (over 9 months up to and including the bleaching event) are inversely related. Seasonal variations in °13C may reflect variations in calcification rate, zooxanthellae photosynthesis or in seawater δ13C composition. Bleached corals had reduced calcification over the 9-month period up to and including the bleaching event and over the event they deposited carbonate enriched in13C and18O compared with unaffected corals. However, calcification during the event was limited and insufficient material was deposited to influence significantly the isotopic signature of the larger seasonal profile samples. In profile, overall decreases in δ18O and δ13C were observed, supporting evidence that positive temperature anomalies caused the bleaching event and reflecting the loss of zooxanthellae photosynthesis.

13C and 18O isotopic disequilibrium in biological carbonates: II. In vitro simulation of kinetic isotope effects

Biological carbonates are built largely from CO2, which diffuses across the skeletogenic membrane and reacts to form HCO−3. Kinetic discrimination against the heavy isotopes 18O and 13C during CO2 hydration and hydroxylation apparently causes most of the isotopic disequilibrium observed in biological carbonates. These kinetic isotope effects are expressed when the extracytosolic calcifying solution is thin and alkaline, and HCO−3 precipitates fairly rapidly as CaCO3. In vitro simulation of the calcifying environment produced heavy isotope depletions qualitatively similar to, but somewhat more extreme than, those seen in biological carbonates. Isotopic equilibration during biological calcification occurs through CO2 exchange across the calcifying membrane and by admixture ambient waters (containing HCO−3) into the calcifying fluids. Both mechanisms tend to produce linear correlations between skeletal δ13C and δ18O.

13C and 18O isotopic disequilibrium in biological carbonates: I. Patterns

Biological carbonates frequently precipitate out of 18O and 13C equilibrium with ambient waters. Two patterns of isotopic disequilibrium are particularly common. “Kinetic” disequilibria, so designated because they apparently result from kinetic isotope effects during CO2 hydration and hydroxylation, involve simultaneous depletions of 18O and 13C as large as 4%. and 10 to 15%., respectively. Rapid skeletogenesis favors strong kinetic effects, and approximately linear correlations between skeletal δ18O and δ13C are common in carbonates showing mainly the kinetic pattern. “Metabolic” effects involve additional positive or negative modulation of skeletal δ13C, reflecting changes in the δ13C of dissolved inorganic carbon, caused mainly by photosynthesis and respiration. Kinetic isotope disequilibria tend to be fairly consistent in rapidly growing parts of photosynthetic corals, and time dependent isotopic variations therefore reflect changes in environmental conditions. δ18O variations from Galapagos corals yield meaningful clues regarding seawater temperature, while δ13C variations reflect changes in photosynthesis, modulated by cloudiness.