The impact of social status on the erythrocyte β-adrenergic response in rainbow trout, Oncorhynchus mykiss

SUMMARYWhen faced with limited resources, juvenile salmonid fish form dominance hierarchies that result in social stress for socially subordinate individuals. Social stress, in turn, can have consequences for the ability of the fish to respond to additional stressors such as pathogens or exposure to pollutants. In the present study, the possibility that social stress affects the ability of rainbow trout (Oncorhynchus mykiss) to tolerate acute increases in water temperature was investigated. To this end, we first evaluated physiological and cellular stress responses following a 1h heat shock in juvenile fish in dominance hierarchies. We measured stress hormone (cortisol and catecholamines) concentrations and blood, brain and liver tissue levels of three heat shock proteins (HSPs), the stress inducible HSP70, the constitutive HSC70 and HSP90, in dominant and subordinate trout. No effects of social status on the hormonal response to the heat stress were detected, but the cellular heat shock response in the brain and liver of dominant and subordinate individuals was inhibited. We then assessed thermal tolerance in dominant and subordinate fish through critical thermal maximum temperature (CT max ) trials and measured HSPs following the heat shock. Subordinate fish were less thermally tolerant than their dominant counterparts. We conclude that social stress impacts the ability of fish to respond, on a cellular scale and in a tissue-specific manner, to increases in water temperature, with likely consequences for overall fitness.

Section: Heat Shocksupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Chronic social stress impairs thermal tolerance in the rainbow trout (Oncorhynchus mykiss)

LeBlanc

Middleton

Gilmour

et al. 2011

“…dominant or high social status versus subordinate or low social status) can impact its physiological status. For example, within pairs of juvenile salmonids, dominant fish tend to exhibit a transient increase in circulating levels of catecholamine (Thomas and Gilmour, 2006) and cortisol [the main glucocorticoid (GC) in teleosts; Øverli et al, 1999] stress hormones during the initial period of hierarchy formation. Dominant fish also exhibit longer-term benefits from the monopolization of food (e.g.…”

Section: Introductionmentioning

confidence: 99%

Programming of the hypothalamic-pituitary-interrenal axis by maternal social status in zebrafish (Danio rerio)

Jeffrey

Gilmour

2016

The present study examined the effects of maternal social status, with subordinate status being a chronic stressor, on development and activity of the stress axis in zebrafish embryos and larvae. Female zebrafish were confined in pairs for 48 h to establish dominant/subordinate hierarchies; their offspring were reared to 144 hours post-fertilization (hpf) and sampled at five time points over development. No differences were detected in maternal cortisol contribution, which is thought to be an important programmer of offspring phenotype. However, once zebrafish offspring began to synthesize cortisol de novo (48 hpf), larvae of dominant females exhibited significantly lower baseline cortisol levels than offspring of subordinate females. These lower cortisol levels may reflect reduced hypothalamic-pituitary-interrenal (HPI) axis activity, because corticotropin-releasing factor (crf) and cytochrome p450 side chain cleavage enzyme (p450scc) mRNA levels also were lower in larvae from dominant females. Moreover, baseline mRNA levels of HPI axis genes continued to be affected by maternal social status beyond 48 hpf. At 144 hpf, stress-induced cortisol levels were significantly lower in offspring of subordinate females. These results suggest programming of stress axis function in zebrafish offspring by maternal social status, emphasizing the importance of maternal environment and experience on offspring stress axis activity.

“…Our findings suggest no adrenergic control over NHE in sablefish RBCs. The concentrations of the adrenergic agonist used in this study have been found to elicit the maximum (saturated) response in rainbow trout blood in vitro (Tetens et al, 1988), but it is also well known that the density and affinity of trout RBC b-adrenergic receptors can be dramatically affected by chronic stress, for example social status or confinement (Thomas and Gilmour, 2006), as well as season and temperature (Koldkjaer et al, 2004;Lecklin et al, 2000). However, we addressed this, in part, by also attempting to activate the bNHE downstream from the adrenergic receptor on the RBC membrane with cAMP (Mahe A 50% air, 0.5% CO 2 , balance N 2 B 0% air, 2% CO 2 , balance N 2 Fig.…”

Section: Rbc Ph Regulationmentioning

confidence: 90%

“…no. 372447) was added to each tonometer to achieve a final nominal concentration of 10 -2 mol l -1 (Mahe et al, 1985;Perry et al, 1996;Thomas and Gilmour, 2006). Additional RBC samples were injected with propranolol (PROP; Sigma-Aldrich cat.…”

Section: Series 2: Rbc Bnhe Activation and Response Characterizationmentioning

confidence: 99%

Use it or lose it? Sablefish,Anoplopoma fimbria, a species representing a fifth teleostean group where the βNHE associated with the red blood cell adrenergic stress response has been secondarily lost

Rummer

Roshan-Moniri

Balfry

et al. 2010

SUMMARYLike most teleosts, sablefish (Anoplopoma fimbria Pallas 1814) blood exhibits a moderate Root effect (~35% maximal desaturation), where a reduction in blood pH dramatically reduces O 2 carrying capacity, a mechanism important for oxygenating the eye and filling the swim bladder (SB) in teleosts. Although sablefish lack a SB, we observed a well-defined choroid rete at the eye. The adrenergically mediated cell swelling typically associated with a functional red blood cell (RBC) b-adrenergic Na + /H + exchanger (bNHE), which would normally protect RBC pH, and thus O 2 transport, during a generalized acidosis, was not observed in sablefish blood. Neither isoproterenol (a b-agonist) nor 8-bromo cAMP could elicit this response. Furthermore, RBC osmotic shrinkage, known to stimulate NHEs in general and bNHE in other teleosts such as trout and flounder, resulted in no significant regulatory volume increase (RVI), further supporting the absence of a functional RBC bNHE. The onset of the Root effect occurs at a much lower RBC pH (6.83-6.92) than in other teleosts, and thus RBC bNHE may not be required to protect O 2 transport during a generalized acidosis in vivo. Phylogenetically, sablefish may represent a fifth group of teleosts exhibiting a secondary reduction or loss of bNHE activity. However, sablefish have not lost the choroid rete at the eye (unlike in the other four groups), which may still function with the Root effect to oxygenate the retina, but the low pH onset of the Root effect may ensure haemoglobin (Hb)-O 2 binding is not compromised at the respiratory surface during a general acidosis in the absence of RBC bNHE. The sablefish may represent an anomaly within the framework of Root effect evolution, in that they possess a moderate Root effect and a choroid rete at the eye, but lack the RBC bNHE and the SB system.