Stress in Atlantic salmon: response to unpredictable chronic stress

Abstract

Combinations of stressors occur regularly throughout an animal's life, especially in agriculture and aquaculture settings. If an animal fails to acclimate to these stressors, stress becomes chronic, and a condition of allostatic overload arises with negative results for animal welfare. In the current study, we describe effects of exposing Atlantic salmon parr to an unpredictable chronic stressor (UCS) paradigm for 3 weeks. The paradigm involves exposure of fish to seven unpredictable stressors three times a day. At the end of the trial, experimental and control fish were challenged with yet another novel stressor and sampled before and 1 h after that challenge. Plasma cortisol decreased steadily over time in stressed fish, indicative of exhaustion of the endocrine stress axis. This was confirmed by a lower cortisol response to the novel stressor at the end of the stress period in chronically stressed fish compared with the control group. In the preoptic area (POA) and pituitary gland, chronic stress resulted in decreased gene expression of 11βhsd2, gr1 and gr2 in the POA and increased expression of those genes in the pituitary gland. POA crf expression and pituitary expression of pomcs and mr increased, whereas interrenal gene expression was unaffected. Exposure to the novel stressor had no effect on POA and interrenal gene expression. In the pituitary, crfr1, pomcs, 11βhsd2, grs and mr were downregulated. In summary, our results provide a novel overview of the dynamic changes that occur at every level of the hypothalamicpituitary gland-interrenal gland (HPI) axis as a result of chronic stress in Atlantic salmon.

Effects of acute and chronic stress on telencephalic neurochemistry and gene expression in rainbow trout (Oncorhynchus mykiss)

“…This is in accordance with our study, showing generally lower plasma cortisol levels in fish held in the highest density for 28 days when exposed to an acute stressor. Madaro et al (2015) reported a similar suppression of HPI-axis reactivity in salmon exposed to repeated unpredictable chronic stress, and they suggested that this type of change was related to increased allostatic load. However, allostatic load may affect HPA/HPI activity in different ways, including decreased resilience and hyperreactivity (Korte et al, 2007;McEwen, 1998).…”

“…For example, the neurodegenerative effects of glucocorticoids in limbic structures are mediated by GRs (for references, see Zhang et al, 2006). In line with this, Madaro et al (2015) suggested that the suppressive effect of chronic stress on GR receptors in teleosts was related to feedback mechanisms protecting against the apoptotic effects of cortisol. Moreover, in mammals, the transcription of the 5-HT 1A receptor gene is negatively regulated by glucocorticoids in the limbic system, an effect that is mediated both by MRs and GRs (Lanfumey et al, 2008).…”

“…Generally, chronic-stress-induced lowering of HPI-axis reactivity seems to be associated with decreased GR1 and GR2 mRNA levels in the POA (Madaro et al, 2015). Furthermore, studies in mammals show that these receptors are involved in allostatic processes.…”

Early life low intensity stress experience modifies acute stress effects on juvenile brain cell proliferation of European sea bass ( D. Labrax )

“…Early life stressful experience in mammals is suggested to control the hypothalamus-pituitary-adrenal (HPA) axis, reducing glucocorticoid receptor (GR) levels at adult age by epigenetic programming of GR promoter [12][13]. Similarly, unpredictable chronic stress in Atlantic salmon resulted in down-regulation of HPI axis and glucocorticoid receptors' mRNAs in the preoptic area [14]. Such changes are in line with the stress concept of allostasis [15][16] that is the adaptive progresses for actively maintaining stability through change.…”

Confirmation that pulse and continuous peracetic acid administration does not disrupt the acute stress response in rainbow trout

“…A reduction in the cortisol response to stress stimuli could, however, be due to different reasons and does not necessarily reflect a process of habituation. For example, the physiological stress responses can become desensitized or exhausted after repeated or chronic exposure to stress (Cyr and Romero, 2009;McKenzie et al, 2012;Barton et al, 2005;Madaro et al, 2015;Moltesen et al, 2016), even when the animals have not habituated to the stressor. Furthermore, different aquatic pollutants are capable of disrupting the normal function of the neuroendocrine pathways involved in the vertebrate stress response, altering the normal synthesis and release of stress hormones such as catecholamines and corticosteroids (Gesto et al, 2008;Ings et al, 2012;Hontela et al, 1997).…”