High temperature stress does not distort the geochemical thermometers based on biogenic calcium carbonate: Stable oxygen isotope values and Sr/Ca ratios of gastropod shells in response to rearing temperature

Abstract

Quantitative profiles of stable isotopes and trace elements in biogenic carbonates have received considerable attention for the purpose of reconstructing past temperatures. The relationships between temperature and the geochemical parameters of carbonates are often subject to both inter- and intraspecific variations, which critically impair the accuracy of temperature estimation. One of the issues that must be addressed to improve temperature estimation is enhancing our understanding of the influence of the kinetic effect. This effect matters because the purely thermodynamic effect to geochemical profiles cannot be effectively separated from the effect of temperature-driven calcification rate. Cowries (Mollusca, Gastropoda, Cypraeidae) may provide a good model system for quantitatively investigating these two effects, because they undergo a callus-building stage in which aragonitic shell formation exclusively occurs to monotonically increase the thickness outward. We reared a total of 230 juvenile individuals of Monetaria annulus under six constant thermal regimes, ranging from the minimum growing temperature (21 °C) to the maximum tolerated long-term temperature (34 °C). The portions of the shells built in the callus-building stage were analyzed to quantify isotopic and elemental compositions. Shell growth rate positively depended on temperature from 21 °C to 33 °C, but dramatically decreased at 34 °C, presumably because of high temperature stress. Nevertheless, the heat stress did not make any impact on the thermal dependences (and among-individual variabilities within the same temperature) of either δ18Oc or Sr/Ca. A linear relationship exists between temperature and the stable oxygen isotope value of the shells (δ18Oc) across the entire thermal range (n = 103), whereas the shell Sr/Ca ratio increased exponentially with increasing temperature (n = 227). These results strongly suggest that any chemical processes responsible for quantitative incorporation of 18O and Sr into aragonite crystals were not impacted by heat stress at temperatures up to 34 °C. Within-temperature residual correlations between shell growth rates and δ18Oc were weakly positive, which is compatible with a widely accepted hypothesis that carbonic anhydrase suppresses the kinetic effect in molluscs. Likewise, we found no association between shell growth rates and Sr/Ca, which rejected the possibility that faster CaCO3 precipitation caused the positive relationship between temperature and Sr/Ca. A large proportion of among-individual variability in shell Sr/Ca was caused by unspecified factors other than temperature. This makes it difficult to accurately estimate the past temperature by measuring the Sr/Ca value of a single shell specimen.