To examine how different fish coping strategies respond to salinity challenge, olive flounder (Paralichthys olivaceus) with active coping style (AC) and passive coping style (PC) were transferred from seawater (SW) to freshwater (FW) and their behavior and physiology were analyzed. Different behavioral coping strategies, in terms of escape and feeding tendencies, were confirmed in AC and PC fish without FW exposure. Differences in swimming distance between AC and PC flounder were then assessed after 1 and 2 days of FW transfer. Plasma parameters and branchial gene expression were also determined 2, 5, 8, and 14 days after transfer, with comparisons between AC and PC fish and against a SW-acclimated control group. The results showed that: (1) PC flounder exhibited a significant reduction in swimming activity, while AC flounder significantly increased locomotion 2 days after transfer. (2) The plasma osmolality and plasma ionic (Na+ and Cl−) concentration of FW-acclimated PC flounder declined in a continuous fashion over time but this contrasted against the plasma parameters of AC flounder which fluctuated below the baseline level of a SW-acclimated control group. (3) The expression of NKA-α1 and NHE-3-like mRNA in PC flounder gill increased significantly from 5 days, but the expression of these two genes in AC flounder only increased after 8 days of transfer. (4) There were no remarkable differences observed in Rhcg expressions between AC and PC flounder. This study indicates for the first time that PC flounder adopt a “freeze-passive tolerance” strategy while AC flounder adopt a “flight-active resistance” defense strategy in response to salinity challenge.

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Stress coping styles are very common in fish, and investigations into this area can greatly improve fish welfare and promote the sustainable development of aquaculture. Although most studies have focused on the behavioral and physiological differences of these fishes, the endocrine response of different coping styles fish when undergoing salinity challenge is still unclear. We examined the physiological response in olive flounder with active coping (AC) style and passive coping (PC) style after transferred from seawater (SW) to freshwater for 0, 2, 5, 8, and 14 days. The results showed that: 1) the plasma prolactin level of FW-acclimated AC flounder was substantially higher than that of FW-acclimated PC flounder at 5, 8, and 14 days, and the branchial gene expression of prolactin receptor (PRLR) in AC flounder was slightly higher than PC flounder after transfer. While there was no remarkable difference observed in cortisol (COR) levels between AC and PC flounder. After transfer, glucocorticoid receptor (GR) expression in AC flounder was significantly higher compared with PC flounder at 8 days. 2) Branchial NKA-IR ionocytes numbers were reduced in PC flounder after transfer, while ionocytes number remain stable in AC flounder. 3) The branchial stem cell transcription factor foxi1 gene expression of AC flounder was significantly higher than PC flounder at 2, 5, and 14 days after transfer, while branchial stem cell transcription factor p63 gene expression of FW-acclimated AC flounder was only substantially higher than that of PC flounder at 5 days. 4) As an apoptosis upstream initiator, the branchial gene expression of caspase-9 in PC flounder was considerably higher than in AC flounder after transfer at 8 days. This study revealed that olive flounder with active and passive coping styles have different endocrine coping strategies after facing the low-salinity challenge. AC flounder adopt an active endocrine strategy by increasing ionocyte differentiation and prolactin secretion significantly. In contrast, PC flounder employ a passive strategy of reducing ionocytes differentiation and retaining prolactin content at a low level to reduce branchial ionocytes number.

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