Freshwater history influences farmed Atlantic salmon (Salmo salar) performance in seawater

The quality of smolts is one of the key factors for successful salmon production. We compared growth performance, physiological traits, and environmental adaptation in Atlantic salmon (Salmo salar) after transfer into a sea cages farm site from recirculating aquaculture system (RAS) to a similar sized group of the same genetic linage and produced in the same husbandry facility but under flow through system (FTS) conditions. Fish vertical distribution within the sea cages and water environment were continuously recorded, while biometry data and biological samples were collected monthly. No significant difference in size and smolt development between the FTS and RAS-produced fish were observed at the end of the freshwater phase. However, after transfer into seawater, the RAS fish showed an array of physiological and molecular differences that were maintained and resulted in significantly increased mortality and lower growth over the full production cycle. The RAS smolts were characterized by lower body weight, length, K factor, HSI (indicator of energy reserve), NKA activity, plasma levels of lactate, triacylglycerol, sodium, calcium, and phosphorus than FTS fish in seawater. This implicated osmoregulatory and allostatic maladaptation for the RAS fish during the first months in seawater. Both FTS and RAS fish showed physiological and behavioral adjustments during the seawater production linked with predictable (e.g., seasonal, diurnal) and short-term unpredictable variation in water temperature and oxygen. However, the RAS fish were characterized by lower physiological response to stressful effects of unpredictable environmental variability.Based on our data, the freshwater history set the basis for the performance success of the FTS and RAS smolts in seawater. FTS fish showed faster adaptation to the seawater environment, with higher osmoregulatory capacity, and higher physiological robustness to seasonal changes than RAS fish, which reflected in their difference in growth and harvest size. We emphasize the crucial role of the freshwater rearing conditions as the foundation for successful physiological adaptation to seawater, growth, and the success of salmon farming production.