Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: Validation of the boron seawater pH proxy

Abstract

Cladocora caespitosa seawater pH pCO 2 Mediterranean ocean acidificationBoron isotopic and elemental systematics are used to define the vital effects for the temperate shallow water Mediterranean coral Cladocora caespitosa. The corals are from a range of seawater pH conditions (pH T~7 .6 tõ 8.1) and environmental settings: (1) naturally living colonies harvested from normal pH waters offshore Levanto, (2) colonies transplanted nearby a subsea volcanic vent system, and (3) corals cultured in aquaria exposed to high (700 μatm) and near present day (400 μatm) pCO 2 levels. B/Ca compositions measured using laser ablation inductively coupled mass spectrometry (LA-ICPMS) show that boron uptake by C. caespitosa cultured at different pCO 2 levels is independent of ambient seawater pH being mainly controlled by temperature-dependent calcification. In contrast, the boron isotope compositions (δ 11 B carb ) of the full suite of corals determined by positive thermal ionisation mass spectrometry (PTIMS) shows a clear trend of decreasing δ 11 B carb (from 26.7 to 22.2‰) with decreasing seawater pH, reflecting the strong pH dependence of the boron isotope system. The δ 11 B carb compositions together with measurements of ambient seawater parameters enable calibration of the boron pH proxy for C. caespitosa, by using a new approach that defines the relationship between ambient seawater pH (pH sw ) and the internally controlled pH at the site of calcification (pH biol ). C. caespitosa exhibits a linear relationship between pH sw and the shift in pH due to physiological processes (ΔpH = pH biol − pH sw ) giving the regression ΔpH Clad = 4.80 − 0.52 × pH sw for this species. We further apply this method ("ΔpH-pH sw ") to calibrate tropical species of Porites, Acropora, and Stylophora reported in the literature. The temperate and tropical species calibrations are all linearly correlated (r 2 N 0.9) and the biological fractionation component (ΔpH) between species varies within~0.2 pH units. Our "ΔpH-pH sw " approach provides a robust and accurate tool to reconstruct palaeoseawater pH sw for both temperate and tropical corals, further validating the boron fractionation factor (α B3-B4 = 1.0272) determined experimentally by Klochko et al. (2006) and the boron isotope pH proxy, both of which have been the foci of considerable debate.

pH homeostasis during coral calcification in a free ocean CO 2 enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef

“…These observations have been independently corroborated by similar measurements of pH cf using electrodes and pH-sensitive dyes (18,21,22). Biological controls on calcification impart significant species-specific but highly systematic increases in pH cf relative to ambient seawater (11). The thermodynamic cost of pH up-regulation within the calcifying fluid, however, is still relatively small compared with the amount of metabolic energy available given normal rates of photosynthesis, respiration, and calcification in reef-building corals (12).…”

“…How sensitive the growth of marine calcifiers is to ocean acidification thus depends on the particular strategies (or lack thereof) for controlling pH at the site of calcification. Based on our findings, we propose three types of strategies: (i) the passive strategy whereby pH up-regulation does not occur and rates of calcification follow an abiotic mineral precipitation curve that is highly dependent on ambient pH and pCO 2 , and growth in these organisms will be highly sensitive (12) to ocean acidification (e.g., some species of foraminifera); (ii) the partial regulation strategy, whereby some up-regulation occurs but the calcifying fluid pH cf is still partially modulated by the external environment (11,12) and rates of calcification are only partially dependent on ambient pH and pCO 2 , and growth in these organisms will be only moderately sensitive to ocean acidification; and (iii) the highly resilient or homeostatic strategy, as identified in this study, where a near constant internal (extracellular) pH cf of the calcifying fluid is maintained at a fixed level to optimize calcification rates independent of external conditions, and growth in these organisms will be the least sensitive to ocean acidification. This homeostasis strategy was also observed in the massive corals Porites lutea and P. lobata during microcosm experiments (37), where the synergetic effects of increased temperature and low pH showed no net effect on calcification rate.…”

“…The boron isotopic composition (δ 11 B) of carbonate skeletons essentially records the biologically mediated pH of the calcifying fluid as calcification occurs (11,12,18). The use of δ 11 B as a pH proxy is based on the selective incorporation of the pH-sensitive and isotopically distinct borate ion, B(OH) 4 , into the corals' calcium carbonate skeleton (19,20).…”

“…Although a clear understanding of the physicochemical mechanisms controlling coral calcification is still only emerging, an important means of biological control is up-regulation of pH (11,12) at the site of calcification (pH cf ). This pH modification is thought to occur predominantly by the biologically mediated action of Ca-ATPase ion transporters that exchange 2H + for Ca 2+ (13,14), but how such biological controls are affected by changes in the ambient marine environment is still poorly understood.…”

Uranium isotope fractionation during coprecipitation with aragonite and calcite

“…If our prediction of the U isotope fractionation during U incorporation into abiotic calcium carbonate in seawater is right, then biological processes may lead to smaller U isotope fractionation during U uptake by biotic CaCO 3 than during abiotic precipitation. Such processes include those that cause changes in (Zeebe et al, 2003;Trotter et al, 2011;Rollion-Bard and Erez, 2009;Nooijer et al, 2009;Al-Horani et al, 2003). The elevation of pH by ~1 unit can lead to significant increase in [CO 3 2-] (~90%, Nooijer et al, 2009 The non-resolvable U isotope fractionation between seawater and modern biogenic carbonates suggests that U isotopes in biotic marine carbonates might be a reliable paleoredox proxy.…”