High sensitivity to ocean acidification in wild out-migrating juvenile Pacific salmon is not impacted by feeding success

Salmon populations are declining worldwide, with high mortality rates during juvenile marine migration presenting a bottleneck to recruitment. The ocean conditions along the main migratory route of juvenile salmon in British Columbia are characterized by high variability in CO₂, with the amplitude, duration, and frequency of ocean acidification events exacerbated by climate change. Similarly, the variability in ocean conditions affects the abundance and diversity of plankton prey, leading to areas of food paucity for juvenile salmon. We investigated the combined effects of ocean acidification (control and 3200 μatm CO₂) and food limitation (ad libitum, ½ ration, and food deprived) on the survival, condition, and gene expression profiles of juvenile Chum salmon (Oncorhynchus keta) to develop predictive biomarkers for CO₂ exposure and food deprivation. Ocean acidification caused a direct 3-fold increase in mortality over 25 days of exposure, which was unaffected by food availability but differentially affected smaller fish. CO₂ exposure induced transcriptomic changes in a suite of genes associated with ion regulation, while food deprivation was associated with a differential expression of stress, immune, and mortality markers, as well as reduced condition factor. Our data indicate that CO₂ directly impairs ionoregulatory capacity to the point of failure in juvenile Chum salmon and that these effects cannot be compensated through increased energy from food. Applying our gene panels as biomarkers to a subset of fish with known exposure, we were able to accurately predict exposure to CO₂ and food deprivation (74% and 90%, respectively). By combining these gene panels with previously established biomarkers for other environmental stressors, the recent environmental stress history of wild fish can be determined and can be used in models to predict salmon returns, informing fisheries management and conservation efforts.