Sea butterflies in a pickle: Reliable biomarkers and seasonal sensitivity of pteropods to ocean acidification in the Gulf of Maine

The passive dissolution of anthropogenically produced CO2 into the ocean system is reducing ocean pH and changing a suite of chemical equilibria, with negative consequences for some marine organisms, in particular those that bear calcium carbonate shells. Although our monitoring of these chemical changes has improved, we have not developed effective tools to translate observations, which are typically of the pH and carbonate saturation state, into ecologically relevant predictions of biological risks. One potential solution is to develop bioindicators: biological variables with a clear relationship to environmental risk factors that can be used for assessment and management. Thecosomatous pteropods, a group of pelagic shelled marine gastropods, whose biological responses to CO2 have been suggested as potential bioindicators of OA owing to their sensitivity to acidification in both laboratory and the natural environment. Using five CO2 exposure experiments, occurring across 4 seasons and running for up to 15 days, we describe a consistent relationship between saturation state, shell transparency, and duration of exposure, as well as identify a suite of genes that could be used for biological monitoring. We clarify variations in thecosome responses due to seasonality, resolving prior uncertainties and demonstrating the range of their phenotypic plasticity. These biomarkers of acidification stress can be implemented into ecosystem models and monitoring programs in regions where pteropods are found, while the approach will serve as an example for other regions on how to bridge the gap between point-based chemical monitoring and biologically relevant assessments of ecosystem health. Summary StatementDespite seasonal variability, pteropods exposed to acidification over multiple seasons reveal consistent patterns in gene expression and shell condition that can be used as bioindicators of ocean acidification stress.