Physiological Causes and Consequences of Social Status in Salmonid Fish

Abstract

Social interactions in small groups of juvenile rainbow trout (Oncorhynchus mykiss) lead to the formation of dominance hierarchies. Dominant fish hold better positions in the environment, gain a larger share of the available food and exhibit aggression towards fish lower in the hierarchy. By contrast, subordinate fish exhibit behavioural inhibition, including reduced activity and feeding. The behavioural characteristics associated with social status are likely the result of changes in brain monoamines resulting from social interactions. Whereas substantial physiological benefits, including higher growth rates and condition factor, are experienced by dominant trout, low social status appears to be a chronic stress, as indicated by sustained elevation of circulating cortisol concentrations in subordinate fish. High cortisol levels, in turn, may be responsible for many of the deleterious physiological consequences of low social status, including lower growth rates and condition factor, immunosuppression and increased mortality. Circulating cortisol levels may also be a factor in determining the outcome of social interactions in pairs of rainbow trout, and hence in determining social status. Rainbow trout treated with cortisol were significantly more likely to become subordinate in paired encounters with smaller untreated conspecifics.

Social descent with territory loss causes rapid behavioral, endocrine, and transcriptional changes in the brain

“…Our work therefore provides novel information on how individuals rapidly adjust their behavior, hormone profile and brain activation patterns when falling in rank. Importantly, this also represents an example of social decline in fishes, which supplements related studies on neural correlates of social subordination in other teleosts such as salmonids (Overli et al, 1999;Gilmour et al, 2005) and zebrafish (Larson et al, 2006;Filby et al, 2010). These studies in fishes, the largest and most diverse group of vertebrates, with >30,000 species, provides crucial and needed comparative data to understand the evolution of coping mechanisms in response to social descent.…”

“…Elevated circulating stress hormones associated with subordinate status occurs in fishes (Fox et al, 1997;Gilmour et al, 2005), reptiles (Summers, 2002) and mammals (Sapolsky, 2005), although in many species, dominant individuals can also have glucocorticoid levels higher than or equivalent to those of subordinates (Creel, 2001;Creel et al, 2013). Cortisol in the bloodstream results from activation of the stress axis in all vertebrates, and serves to direct metabolic energy away from long-term physiological processes such as reproduction and focus it towards shorter-term goals of combating the stressor (McEwen and Seeman, 1999).…”

Chronic cortisol and the regulation of food intake and the endocrine growth axis in rainbow trout

“…For example, chronic exposure to aluminum, copper, selenium or low environmental pH can result in prolonged elevations in plasma cortisol levels (Craig et al 2009, Wiseman et al 2011, Kennedy & Picard 2012, Grassie et al 2013. In salmonids, sustained increases in cortisol levels are also associated with social subordination (Gilmour et al 2005) and with specific phases of the life cycle such as smolting (Nilsen et al 2008) and sexual maturation (Fuzzen et al 2011). In fact, plasma cortisol levels can reach several hundred ng/ml and remain elevated for weeks to months in sexually mature and migrating Pacific salmon (Carruth et al 2000, Hinch et al 2006, Westring et al 2008.…”

The interrenal gland in males of the cichlid fish Cichlasoma dimerus: Relationship with stress and the establishment of social hierarchies

“…Many studies have evaluated the relationship between social context and the neuroendocrine axes involved in the stress response in teleosts (Alonso et al, 2012;DiBattista et al, 2005;Earley et al, 2006;Fox et al, 1997;Gilmour et al, 2005;Sørensen et al, 2011Sørensen et al, , 2012. In general, dominant individuals hold the highest position within the social hierarchy, taking possession of valuable resources related to food, reproduction or defense (Chichinadze and Chichinadze, 2008;Sloman et al, 2000), whereas subordinate individuals are excluded from all or some of them; aggression is, in most of the cases, an essential prerequisite for the establishment of social hierarchies (Desjardins et al, 2012;Parikh et al, 2006;Sloman et al, 2000).…”