Physiological and isotopic responses of scleractinian corals to ocean acidification
Introduction
Atmospheric CO2 concentration has increased from pre-industrial levels of 280 ppmv to over 380 ppmv, the highest concentration over the last 800,000 years (Luthi et al., 2008). By the end of this century, atmospheric CO2 concentration is predicted to double relative to pre-industrial levels as a direct result of human activity (Solomon et al., 2007). Approximately a quarter of anthropogenic CO2 is being absorbed by the ocean (Sabine et al., 2004, Canadell et al., 2007), and at the current rate of CO2 uptake the average surface ocean pH will drop from 8.2 to 7.8 by the end of 2100 (Caldeira and Wickett, 2005). This represents a shift in seawater pH to levels below those experienced by marine organisms during the last several million years (Pearson and Palmer, 2000). The associated decrease in seawater carbonate ion concentration [] could substantially impact calcifying organisms, such as scleractinian corals, by lowering the saturation of ocean water with respect to the carbonate mineralogy of their skeletons (Gattuso et al., 1998, Kleypas et al., 1999a, Leclercq et al., 2000, Orr et al., 2005, Schneider and Erez, 2006, Anthony et al., 2008, Marubini et al., 2008). The aragonite saturation state (Ωarag) is defined as:where is the apparent solubility product of the mineral. Values of Ωarag > 1 indicate supersaturation, whereas Ωarag < 1 is undersaturated. Coral reefs in the modern ocean are restricted to regions where seawater Ωarag exceeds 3.3 (Kleypas et al., 1999b). Modeling of future Ωarag indicates that by 2040 surface waters in regions like the Australian Great Barrier Reef will become marginal for coral calcification (Kleypas et al., 2006) potentially threatening the existence of these unique ecosystems.
Accurate predictions of the viability of coral reef ecosystems under conditions of ocean acidification require information on how coral physiology and calcification will respond (Kleypas et al., 2006). In particular, the effect of ocean acidification on the relationship between the symbiotic photosynthetic algae (zooxanthellae) contained within the tissue of most coral and the calcification of the coral’s aragonite skeleton. Zooxanthellae activity strongly stimulates calcification; during daylight, when the algae are photosynthesizing, calcification rates are 3–4 times greater than in the dark (Gattuso et al., 1999, Furla et al., 2000). However, the explanation for how zooxanthellae photosynthesis and coral calcification are connected remains controversial (Muscatine, 1990, Gattuso et al., 1999, Cohen and McConnaughey, 2003, Schneider and Erez, 2006).
In this study, we have investigated the response of scleractinian reef-forming corals and their zooxanthellae after long-term (up to 14 months) exposure to normal and reduced pH conditions (8.09, 7.49, and 7.19 on the pHT scale). Corals in the low-end pH treatment were exposed to extremely high pCO2 (equivalent to seven times the predicted CO2 level by 2100), to investigate the physiological response at Ωarag < 1 and its translation into skeletal C, O, and B isotopic signatures. Two zooxanthellate coral species with very different life strategies were studied to provide information on the range of potential responses. The massive Porites sp. form large multi-century old colonies and calcify relatively slowly (extending 1–2 cm yr−1), whereas the branching Stylophora pistillata is short-lived and deposits skeleton rapidly. The responses of both species to shifts in CO2 and seawater carbonate chemistry were monitored using isotopic tracers (skeletal δ11B, δ13C, and δ18O, and coral tissue and zooxanthellae δ13C) and key physiological parameters including skeletal growth, tissue biomass, zooxanthellae cell density, and chlorophyll concentration.
The isotopic systems (δ11B, δ18O, and δ13C) investigated in this study are often used as palaeo-environmental proxies. Skeletal δ18O is the most commonly used proxy for seawater temperature and salinity (Cole et al., 2000, Gagan et al., 2000, Hendy et al., 2002, Al-Rousan et al., 2003, Asami et al., 2004, Linsley et al., 2006). Skeletal, tissue, and zooxanthellae δ13C has been used to trace seawater carbonate chemistry and metabolic processes that cause preferential addition or subtraction of 12C from the internal DIC pool through respiration and photosynthesis (Risk et al., 1994, McConnaughey et al., 1997, Grottoli, 1999, Grottoli, 2002, Grottoli and Wellington, 1999, Heikoop et al., 2000, Asami et al., 2004, Swart et al., 2005, Omata et al., 2008). ‘Vital effects’ during the biomineralization of the coral skeleton have been observed to shift both δ13C and δ18O values (McConnaughey, 1989b, Allison et al., 1996, Heikoop et al., 2000, Omata et al., 2008). Since many potential sources of ‘vital effects’ are pH sensitive physiological processes (e.g., zooxanthellae photosynthetic activity, polyp metabolism, calcification rate), ocean acidification may also affect these skeletal isotopic tracers. Investigations into the effect of seawater pH on coral δ18O and δ13C are limited and there are no studies of species-specific variation of δ18O and δ13C in a controlled pCO2 system.
Reconstruction of past seawater pH levels may assist in understanding future impacts of reduced oceanic pH on corals and their resilience to ocean acidification. The boron isotopic composition (δ11B) of marine carbonates is used as a proxy for reconstructing paleo-pH, as applied in studies of experimentally cultured (Hönisch et al., 2004, Reynaud et al., 2004) and retrieved corals (Hemming and Hanson, 1992, Hemming et al., 1998, Pelejero et al., 2005, Kasemann et al., 2009, Wei et al., 2009). The relative concentration of boric acid [B(OH)3] and the borate ion [], the two main boron species in the ocean, is pH dependent and there is a ∼27‰ difference in δ11B between these two species (Klochko et al., 2006). Environmental variables such as water temperature, irradiance, food supply, and water depth have been shown to have little effect on bulk δ11B values of coral skeleton (Hönisch et al., 2004, Reynaud et al., 2004). However, ‘vital effects’ have been implicated in micron-scale skeletal δ11B variations measured in both deep-sea (i.e., non-zooxanthellate) and shallow-water (i.e., zooxanthellate) corals by Secondary Ion Mass Spectrometry (SIMS) (Rollion-Bard et al., 2003, Blamart et al., 2007). As a result, fundamental questions remain regarding the degree to which bulk B isotopic compositions of shallow-water scleractinian corals correlate with changes in water pH and the degree to which species-dependent ‘vital effects’ perturb this relationship (Hönisch et al., 2004, Blamart et al., 2007).
Section snippets
Experimental design
Two colonies of Porites sp. and four colonies of S. pistillata were collected in July 2007 from the reef in front of the Interuniversity Institute for Marine Science in Eilat, Israel (IUI) (29°30′N, 34°55′E), at 8 m depth. Following fragmentation, pieces were glued to pre-labeled glass slides. After a one-month recovery period the fragments were dyed with Alizerine Red (Sigma–Aldrich, USA) in order to mark the beginning of the experiment in the skeleton, and 20 fragments of each species were
Results
All corals survived throughout the 14 months of the experiment and new skeletal growth was observed on the glass slides under all three experimental conditions. We also note that corals from the same batch, which were not harvested, are still alive and continue to add skeletal material at the time this paper was written, 28 months after the beginning of the experiment.
Acclimatization to high pCO2
Stylophora pistillata and massive Porites sp. fragments were exposed to pCO2 levels of up to sevenfold higher than those predicted to prevail by the end of this century. Following 14 months incubation under reduced pH conditions (8.09, 7.49, and 7.19), all coral fragments survived and added new skeletal calcium carbonate, despite Ωarag values as low as 1.25 and 0.65 (Table 1). These findings suggest that scleractinian coral species will be able to acclimate to a high pCO2 ocean even if changes
Conclusions
The long acclimation time of this study allowed the coral colonies to reach a steady state in terms of their physiological responses to elevated pCO2. As a result, the physiological response to higher pCO2/lower pH conditions was significant, but less extreme than reported in previous experiments. Our findings suggest that scleractinian coral species will be able to acclimate to a high pCO2 ocean even if changes in seawater pH are faster and more dramatic than predicted. Although skeletal
Acknowledgments
The authors thank Murielle Dray for technical assistance, Irena Brailovsky for assistance with isotopic analysis at the Weizmann Institute, and Simon Berkowicz and Lena Hazanov for comments on an early version of the manuscript. The authors also thank the staff of the Interuniversity Institute for Marine Sciences in Eilat for the technical support throughout the experiment and the members of the Bristol Isotope Group (BIG), University of Bristol. This work was supported by the UK Natural
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