Carbon isotopes in mollusk shell carbonates

Mollusk shells contain many isotopic clues about calcification physiology and environmental conditions at the time of shell formation. In this review, we use both published and unpublished data to discuss carbon isotopes in both bivalve and gastropod shell carbonates. Land snails construct their shells mainly from respired CO2, and shell δC reflects the local mix of C3 and C4 plants consumed. Shell δC is typically >10‰ heavier than diet, probably because respiratory gas exchange discards CO2, and retains the isotopically heavier HCO3 . Respired CO2 contributes less to the shells of aquatic mollusks, because CO2/O2 ratios are usually higher in water than in air, leading to more replacement of respired CO2 by environmental CO2. Fluid exchange with the environment also brings additional dissolved inorganic carbon (DIC) into the calcification site. Shell δC is typically a few‰ lower than ambient DIC, and often decreases with age. Shell δC retains clues about processes such as ecosystem metabolism and estuarine mixing. Ca ATPase-based models of calcification physiology developed for corals and algae likely apply to mollusks, too, but lower pH and carbonic anhydrase at the calcification site probably suppress kinetic isotope effects. Carbon isotopes in biogenic carbonates are clearly complex, but cautious interpretation can provide a wealth of information, especially after vital effects are better understood. Introduction Over the past half century, isotopic geochemists have extracted a plethora of information on paleotemperatures and hydrological processes from the oxygen isotope compositions (δO) of biogenic carbonates (e.g., Emiliani 1954, and many others since). The carbon isotopic compositions (δC) of shell and bone carbonates have also yielded useful information, but uncertainty concerning the origins of carbonate carbon has remained a problem. When does calcification draw mainly from respired CO2, derived from food? When does inorganic carbon from ambient air or water dominate? How does carbon reach the calcification site? Does the phylogenetic position, physiology, or ecology of the calcifying animal matter? Resolving such questions will improve reconstructions of past CO2 levels, the mixing of marine and fresh waters, animal diets, upwellings, ecological upheavals, and many other aspects that geochemists, paleontologists, ecologists, and archaeologists study using biogenic carbonate δC. This analysis focuses on mollusks. But just as mice, nematodes and bacteria provide insights into human physiology and medicine, so too do non-mollusks provide insights into mollusks. Scientists will also want to apply insights gained from mollusks to other animals. Numerous comparisons between mollusks and other organisms are therefore included, but we always return to mollusks to discuss the strengths and weaknesses of the evidence in this group. Mollusks make attractive environmental recorders because of their abundance in diverse environments, and their sequential skeletal deposition. Developmental or ontogenetic changes can, however, affect isotopic fractionations. This opens opportunities for monitoring the animal, but Geo-Mar Lett (2008) 28:287–299 DOI 10.1007/s00367-008-0116-4 T. A. McConnaughey 2906 Norman Dr., Boise, ID 83704, USA D. P. Gillikin (*) Department of Earth Science and Geography, Vassar College, P.O. Box 475, Poughkeepsie, NY 12604, USA e-mail: [email protected] complicates environmental monitoring. Understanding ‘vital’ effects is therefore important for distinguishing physiological from environmental factors. Recent insights have emerged from detailed measurements on common animals, plus examination of animals from unusual environments. Subtle differences in calcification physiology now appear to account for markedly different isotopic outcomes. Respired CO2 and ambient inorganic carbon both contribute to mollusk shells, and the relative importance of each source will determine whether shell δC records mainly dietary δC, or the δC of ambient inorganic carbon. McConnaughey et al. (1997) suggested that land snails and other air-breathing animals build their carbonates mainly from respired CO2, while aquatic animals build their shells mainly from ambient inorganic carbon. We reexamine this issue, discuss some physiological environmental factors that affect the balance of carbon sources, and offer new insights into the observed isotopic fractionations. This paper emphasizes generalizations that work for large parts of nature, the processes that give rise to these generalizations, and reasons why they sometimes fail. Many fundamental issues have not been settled. Highlighting these uncertainties may help geochemists, paleontologists, and archaeologists to recognize and avoid some common pitfalls, and will hopefully encourage basic research. Carbon isotopes in biogenic carbonates are clearly complex, but cautious interpretation can provide a wealth of information. Calcification physiology Various mollusks construct their shells of calcite, aragonite, or both (Fig. 1a). Calcification occurs from the extrapallial fluid (EPF), which is often divided into inner and outer sections (Wilbur and Saleuddin 1983; Wheeler 1992). Sampling these fluids is technically difficult due to their small volumes, and most chemical measurements have been made from the inner EPF (Crenshaw 1972; Wada and Fujinuki 1976; Lécuyer et al. 2004; Ip et al. 2006), rather than the outer EPF (Lorens 1978). The inner EPF produces the inner shell layer, and geochemical studies have concentrated on the outer shell layer for better timeresolved records (see Vander Putten et al. 2000). Outer EPF fluids have not been sampled for isotopes, although there is one report of oxygen isotopes from inner EPF (Lécuyer et al. 2004). Nevertheless, Gillikin et al. (2005a) found similar δC and δO in the inner and outer shell regions. Rapid calcification from the EPF indicates that it is significantly supersaturated with respect to CaCO3. Hence, mollusks presumably add Ca or CO3 , or both to the EPF. Studies have observed only minor differences between inner EPF fluids, hemolymph fluids, and ambient seawater with respect to Ca levels, and ratios of Ca to Mg, Sr, and Ba (Wada and Fujinuki 1976; Lorrain et al. 2004a; Gillikin 2005; Gillikin et al. 2006a). This seems consistent with passive conduction of ions to the calcification site, perhaps by pericellular routes through the mantle, Fig. 1 a Cross section through a mussel shell (morphology from Vander Putten et al. 2000), showing likely transport routes for calcium and inorganic carbon. bModel depicting Ca and CO3 = concentrations, and aragonite saturation level Ω in seawater, modified by Ca/2H exchange and CO2 dissolution. CO3 =K1K2[CO2]/{H }, Ca calculated from alkalinity. c Fractions of skeletal carbon supplied as CO2 from mantle, and Ca pumped from the mantle cells, calculated for seawater (pH 8, pCO2=atmospheric), and for freshwater Crystal Pool NV (pH 7.3, pCO2=23×atmospheric). The balance of skeletal carbon and calcium presumably derives from fluid exchange with ambient waters, by leakage around the edge of the shell, or through mantle tissues. Based on the model of Cohen and McConnaughey (2003) 288 Geo-Mar Lett (2008) 28:287–299