Energetic Costs of Acidification, Hypoxia, and Warming in Early Life Stages of a Coastal Fish

Responses of fish to environmental stressors can vary by life stage, with the early life stages often showing more sensitivity. It is important to account for this when measuring biological responses to multiple stressors in a laboratory setting, and when modeling whole-organism energy budgets. Dynamic energy budget (DEB) theory incorporates the differing energetic inputs and demands of each life stage, and thus is an ideal framework for scaling organismal responses to acidification up to the population level. A DEB model for Atlantic silversides (Menidia menidia) was built using physiological measurements taken on embryos, larvae, and juveniles, primarily from a series of experiments rearing offspring in factorial combinations of carbon dioxide (CO₂), temperature, and dissolved oxygen levels. The treatments were designed to simulate current and end-of-century levels for estuaries in the Northeast United States. Growth, survival, metabolic rates, and ionocyte abundance were measured and used in the DEB model, and metabolism and ionocyte results are presented here. We hypothesized that ocean acidification due to elevated CO₂ would increase the energetic costs of homeostasis through the added need for acid-base balance, and that ionocyte abundance on the skin and gills would increase. We also hypothesized that CO₂ would interact with the other stressors and modify the fish’s response to high temperature and hypoxia. In experiments combining temperature and CO₂ treatments, temperature significantly affected metabolic rates in silverside embryos and larvae but CO₂ did not. There were significant interactions between temperature and CO₂ on ionocyte abundance in larvae, and the response of ionocytes to acidification depended on timing in the spawning season. Dissolved oxygen (levels of 8, 4, and 3 mg/L) and CO₂ interacted such that embryo metabolic rates decreased with hypoxia under elevated CO₂ but not ambient CO₂. This effect was absent in larvae. The stage-specific responses we found demonstrate the value of using a DEB model to conceptualize the effects of multiple stressors on energy budget and to make population growth predictions based on energetic costs of stressors.