Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness

The aim of this study was to establish whether two lines of rainbow trout divergent for their plasma cortisol response to a standardized stressor would show consistent differences in their behavioural response to a range of challenging situations. Our results show that the high- and low-responding (HR and LR) lines of rainbow trout did not differ in the aggression shown towards an intruder or in their response to the introduction of a novel object to their home environment. However, there was a difference in behaviour between the two selection lines when they were exposed to two unfamiliar environments. These results suggest that the behaviour of the HR and LR fish differs when they are challenged in unfamiliar environments, while their behaviour does not differ when they are challenged in their home environment. These observations are in agreement with studies on mammals that show that individuals with reactive coping styles perform similarly to proactive animals when they are challenged in a familiar environment, while they show different behaviour when they are challenged in unfamiliar environments. Thus, these results provide further evidence that the HR and LR selection lines of rainbow trout exemplify the two different coping styles described in mammals

Dietary l-tryptophan leaves a lasting impression on the brain and the stress response

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Stress Coping Strategies in Rainbow Trout (Oncorhynchus mykiss)

Animals show a great variety in physiological and behavioural responses to stressors. These responses are often bimodally distributed within populations and show consistency on an individual level over time and across situations, which in terrestrial vertebrates have been identified as proactive and reactive stress coping strategies. Proactive animals show lower cortisol responses, higher sympathetic activation and brain serotonergic activity compared to reactive animals. Behaviourally, proactive animals are more aggressive, more active in avoiding stressors, they form routines and show fewer cases of conditioned immobility compared to reactive animals. Our aim has been to reveal if such stress coping strategies exist in fish. Our results show that rainbow trout with high (HR) or low (LR) cortisol responses to stressors differs in sympathetic activation and brain serotonin turnover in the same manner as proactive and reactive mammals. HR fish showed less locomotor activity when reared in large groups (30 individuals) compared to LR fish. When reared in isolation there were no differences between HR and LR fish when exposed to stressors within a familiar environment. The adaption of a proactive coping style among reactive coping individuals when they are challenged within a familiar environment has previously been shown to be distinction between proactive and reactive coping mammals. However, when they were transferred to unfamiliar environments a behavioural difference between the two lines was observed indicating different stress coping strategies akin to those described in mammals. Finally, we observed a consistency over time in the cortisol response of an unselected line of rainbow trout. Fish from this line also demonstrated a correlation between behavioural responses to different stressors. However, there was no apparent connection between these behavioural responses and the cortisol response. Overall, the results of this thesis have strengthened the hypothesis that different stress coping strategies exist in teleost fish

Stress and stress coping in fish, behavioural correlates and neuroendocrine mechanisms

The development of a dominance based social hierarchy is common among teleost fish and individual social history greatly affects physiology and behaviour of the fish. Long-term social subordination inhibits aggressive behaviour and predisposes the fish for losing subsequent fights for social dominance, whereas experience of being dominant, has the opposite effect, making the fish more likely to win future encounters. Subordinate individuals are exposed to chronic stress and show a chronic activation of the hypothalamic-pituitary-interrenal (HPI) axis and the brain serotonergic system. Elevated brain serotonergic activity is important for mediating the behavioural inhibition observed in subordinate fish. However, cortisol and neuropeptides involved in the control of the HPI axis also seem to play important roles in mediating behavioural effects of social experience. Moreover, in rainbow trout (Oncorhynchus mykiss), competitive ability is linked to suite of other behavioural traits and to the neuroendocrine stress response profile. Trout responding to stress with a low increase in plasma cortisol have an advantage in dyadic fights for social dominance with a conspecific responding to the same stressor with a larger increase in plasma cortisol. Moreover, rainbow trout selectively bred for low post-stress plasma cortisol (LR trout) have an advantage over trout selected for high post-stress cortisol (HR trout) in dyadic encounters. Thus, in addition to the epigenetic effects of social history there are also genetic factors predisposing individuals for dominant and subordinate social positions

Does individual variation in stress responsiveness and behavior reflect divergent stress coping strategies in rainbow trout?

In rainbow trout (Oncorhynchus mykiss) the magnitude of the cortisol response to stress shows both consistency over time and a high degree of heritability, and high responding (HR) and low responding (LR) lines of rainbow trout has been generated by individual selection for consistently high or low post-stress cortisol values (Pottinger and Carrick, 1999). In addition to divergent post-stress plasma levels of cortisol, HR and LR trout also differ in other neuroendocrine parameters. For instance, LR fish show higher brain serotonin (5-Hydroxytryptamine, 5-HT) turnover (Øverli et al., 2001), and respond to acute stress with a larger increase in plasma catecholamines, than HR fish do. Moreover, a link between neuroendocrine stress responses and behavioural traits is evident from observations on these lines of rainbow trout. In particular, LR fish are socially dominant over HR fish when paired (Pottinger and Carrick, 2001). LR trout also resume feeding faster than HR trout when transferred to social isolation, and display a reduced locomotor response in a territorial intrusion test (Øverli et al., 2002a). When kept in groups LR fish show higher locomotor activity than HR fish, a difference that could be related to higher levels of aggression in groups of LR fish. A higher level of aggression in LR fish is also suggested by the fact that LR fish grew faster than HR fish when kept in mixed groups. The combination of these results suggests that LR and HR trout are displaying divergent stress coping styles, LR fish being proactive and HR fish reactive (Koolhaas et al., 1999). Recent results from similar studies using a non-selected hatchery population of rainbow trout supports the suggestion that divergent stress coping strategies, akin to what has been described as proactive and reactive stress coping in rodents (Koolhaas et al., 1999), exists in rainbow trout. A reciprocal relationship between the brain and endocrine system appear to exist, linking cortisol levels during stress to behavioural traits such as the outcome of agonistic interactions. Data from other studies suggest that the brain 5-HT system could provide such a link between stress responses and behaviour. In salmonid fish, as in many other vertebrates, social subordination results in a drastic but reversible inhibition of behavioural responsiveness along with a sustained activation of the brain 5-HT system. Elevated brain 5-HT activity appears important in mediating several behavioural and physiological responses to social subordination, including inhibition of aggressive behaviour, lowered feed intake, suppression of locomotor activity and elevated plasma cortisol levels (Winberg and Nilsson, 1993). However, cortisol may also have behavioural effects, as well as effects on the synthesis and release of 5-HT and other monoaminergic neurotransmitters. We have shown that short-term cortisol treatment increases activity and aggression whereas long-term treatment with cortisol has the opposite effect, decreasing activity and aggression in rainbow trout (Øverli et al., 2002b). Thus, cortisol appears to have time- and context-dependent effects on behaviour, which could either be mediated by interaction with 5-HT or other neurotransmitter systems, or reflect a direct behavioural role for cortisol receptors in fish

Blood and plasma parameters.

<p>Mean values (± SEM) of haematocrit (a), plasma chloride (b), plasma sodium, (c), water content in muscle tissue (d), plasma lactate (e), and blood ethanol (f) in crucian carp after 2, 6, 10 and 14 days of exposure to the acidic Al-rich water (closed circles), acidic Al-poor water (open circles) and untreated department water (open squares). n = 7 if not noted differently on the graph. Time points within experimental groups assigned with different letters are significantly different from each other (p < 0.05). Experimental groups assigned with asterisks (*) displayed significant differences (p<0.05) in comparison to the other two groups. Experimental groups assigned with asterisks in brackets ([*]) displayed a significant difference in physiological parameters in comparison to only one of the other groups (also assigned with [*]). All data are listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0179519#pone.0179519.s003" target="_blank">S3 Table</a>.</p

pH, temperature and conductivity in the various waters used in the experiments.

<p>pH, temperature and conductivity in the various waters used in the experiments.</p

Al-concentrations (μg/l) in the various waters used in the experiments.

<p>Al-concentrations (μg/l) in the various waters used in the experiments.</p