Metabolic proxy for cephalopods: Stable carbon isotope values recorded in different biogenic carbonates

Abstract

Measuring the metabolic rate of marine animals in their natural environment is challenging, impeding our understanding of their physiological ecology. Recently, a novel metabolic proxy, namely the delta C-13 values of biogenic carbonates (otoliths), was experimentally validated in teleost fishes. Cephalopods possess several types of biogenic carbonates, such as statolith, cuttlebone and other internal and external shells, which are all potential metabolic recorders, but few have been evaluated. To test the feasibility of the delta C-13 metabolic proxy in cephalopods, we conducted a temperature-controlled experiment with the pharaoh cuttlefish Sepia pharaonis to assess whether the proportion of metabolically derived carbon (C-resp) incorporated into statoliths and cuttlebones increases with metabolism in a warm environment. Moreover, we conducted multiple-species analysis using the published delta C-13 values of various biogenic carbonates to evaluate the consistency of the proxy among cephalopod species and between cephalopods and teleost fishes. In the temperature-controlled laboratory experiment, C-resp values calculated from statoliths and cuttlebones increased with an increase in environmental temperature. C-resp values did not differ between statoliths and cuttlebones. Moreover, the C-resp values of cephalopod biogenic carbonates had a similar range to those of fish otoliths and were correlated with metabolism-related factors, such as ambient temperature, body mass, ontogeny and functional behaviours, strengthening the feasibility of their use. The delta C-13 metabolic proxy reflects the total energy use in the natural environment, and it can be transformed into the oxygen consumption rate for a broader comparison with other species and for further evaluation with current theories related to metabolic ecology. However, experimental validation is highly recommended because the relationship between the oxygen consumption rate and C-resp values derived from biogenic carbonates of cephalopods might be structure- and species-specific. Our study revealed that the newly developed metabolic proxy provides a valuable alternative approach to study ecophysiology in cephalopods, and further development might broaden its applicability.