Abstract
Ensuring salmon health and welfare is crucial to maximize production in recirculation aquaculture systems. Healthy and robust mucosal surfaces of the skin and intestine are essential to achieve this goal because they are the first immunological defenses and are constantly exposed to multistressor conditions, such as infectious diseases, suboptimal nutrition, and environmental and handling stress. In this work, Atlantic salmon, split from a single cohort, were subjected to acute hypoxia stress or 15-min crowding stress and observed over a 24-h recovery period. Samples were collected from fish at 0, 1, 3, 6, 12 and 24 h post-stress to analyze plasma-circulating markers of endocrine function (cortisol), oxidative stress (glutathione peroxidase) and immune function (interleukin 10 (IL-10), annexin A1). In addition, mucosal barrier function parameters were measured in the skin mucus (Muc-like protein and lysozyme) and distal intestine (simple folds, goblet cell size and goblet cell area). The results showed that both acute stress models induced increases of circulating cortisol in plasma (1 h post-stress), which then returned to baseline values (initial control) at 24 h post-stress. Moreover, the hypoxia stress was mostly related to increased oxidative stress and IL-10 production, whereas the crowding stress was associated with a higher production of Muc-like protein and lysozyme in the skin mucus. Interestingly, in the distal intestine, smaller goblet cells were detected immediately and one hour after post-hypoxia stress, which could be related to rapid release of the cellular content to protect this organ. Finally, the correlation of different markers in the hypoxic stress model showed that the circulating levels of cortisol and IL-10 were directly proportional, while the availability of Muc-like proteins was inversely proportional to the size of the goblet cells. On the other hand, in the crowding stress model, a proportional relationship was established between plasma cortisol levels and skin mucus lysozyme. Our results suggest key differences in energy partitioning between the two acute stress models and support the need for further investigation into the interplay of multistressor conditions and strategies to modulate immunological aspects of mucosal surfaces.
Highlights
Continuous growth of the aquaculture industry and implementation of recirculating aquaculture systems (RAS), where fish are kept in a closed environment during the whole production cycle, raise concerns with regard to fish welfare, health and growth potential [1,2]
The results concerning plasma cortisol (Figure 1A) from the initial control fish group showed an average of 85.40 ± 71.06 ng mL−1, while fish subjected to hypoxia and crowding stress demonstrated changing cortisol levels compared with the initial control
The levels of cortisol subsequently declined significantly compared with the hypoxia group at 6 h post-stress
Summary
Continuous growth of the aquaculture industry and implementation of recirculating aquaculture systems (RAS), where fish are kept in a closed environment during the whole production cycle, raise concerns with regard to fish welfare, health and growth potential [1,2]. Fish management practices can involve multiple stressful conditions (chemical, biological, physical and procedural) that can affect the responses of mucosal surfaces as the first defense barriers against biological challenges [1,2,3,4]. Stress response assessment is a complex topic and measuring and interpreting the results is not always clear for a variety of reasons, including differences in stress model procedures among experiments [6]. There are numerous studies that have looked at different stress models and evaluated stress responses at diverse levels [7,8,9,10,11]. Few studies have performed side-by-side characterizations of acute stress effects on mucosal tissues such as skin and intestine
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