Identification of food deprivation in salmonids using gill biomarkers

Risk assessments have identified prey limitation as one of the strongest risk factors for juvenile salmon survival under climate change. In British Columbia, Canada, juvenile Chinook salmon (<i>Oncorhynchus tshawytscha</i>) may experience prolonged periods of food deprivation upon marine entry and during their first marine winter. We assessed the physiological and transcriptional consequences of food deprivation to discover and develop mRNA-based biomarkers for food deprivation in the gill of juvenile Chinook salmon. Gill and liver tissue were collected from juvenile Chinook salmon held at 16 or 8°C that were fed or food deprived for up to 56 days and during a 21-day refeeding period. Chinook salmon at 16 and 8°C were able to withstand food deprivation for periods of 35 and 56 days, respectively, with declines in body morphometrics, hepatosomatic index, insulin-like growth factor-1 and energy density observed in food-deprived individuals, followed by rapid recovery during refeeding. RNA-sequencing at the end of the food deprivation period revealed candidate biomarkers for food deprivation representing structural and functional components of the gill as well as metabolic processes like lipid storage and energy metabolism in the liver. Using the strongest 12 gill biomarkers paired with high-throughput qPCR and a random forest classification model, transcriptional signatures of food deprivation were detected within 14 to 28 days following food deprivation and persisted for at least 6 days following refeeding. These gill biomarkers can be non-lethally applied to wild juvenile salmon to answer long standing questions regarding food deprivation and the drivers of mortality during their early marine migration and overwintering.