Ocean acidification exerts negative effects during warming conditions in a developing Antarctic fish

Anthropogenic CO2 is rapidly causing oceans to become warmer and more acidic, challenging marine ectotherms to respond to simultaneous changes in their environment. While recent work has highlighted that marine fishes, particularly during early development, can be vulnerable to ocean acidification, we lack an understanding of how life-history strategies, ecosystems and concurrent ocean warming interplay with interspecific susceptibility. To address the effects of multiple ocean changes on cold-adapted, slowly developing fishes, we investigated the interactive effects of elevated partial pressure of carbon dioxide (pCO2) and temperature on the embryonic physiology of an Antarctic dragonfish (Gymnodraco acuticeps), with protracted embryogenesis (∼10 months). Using an integrative, experimental approach, our research examined the impacts of near-future warming [-1 (ambient) and 2°C (+3°C)] and ocean acidification [420 (ambient), 650 (moderate) and 1000 μatm pCO2 (high)] on survival, development and metabolic processes over the course of 3 weeks in early development. In the presence of increased pCO2 alone, embryonic mortality did not increase, with greatest overall survival at the highest pCO2. Furthermore, embryos were significantly more likely to be at a later developmental stage at high pCO2 by 3 weeks relative to ambient pCO2. However, in combined warming and ocean acidification scenarios, dragonfish embryos experienced a dose-dependent, synergistic decrease in survival and developed more slowly. We also found significant interactions between temperature, pCO2 and time in aerobic enzyme activity (citrate synthase). Increased temperature alone increased whole-organism metabolic rate (O2 consumption) and developmental rate and slightly decreased osmolality at the cost of increased mortality. Our findings suggest that developing dragonfish are more sensitive to ocean warming and may experience negative physiological effects of ocean acidification only in the presence of an increased temperature. In addition to reduced hatching success, alterations in development and metabolism due to ocean warming and acidification could have negative ecological consequences owing to changes in phenology (i.e. early hatching) in the highly seasonal Antarctic ecosystem.