Perhaps the best documented physiological consequence of subordinate social status in salmonid fish is a reduction in growth rate (e.g., Li and Brocksen, 1977
; Metcalfe, 1986; Abbott and Dill, 1989; Metcalfe et al., 1990; Pottinger and Pickering, 1992; Ryer and Olla, 1996; Sloman et al., 2000b, 2001b, 2002c). The lower growth rates of subordinate fish stem, at least in part, from reduced food intake owing to monopolisation of food sources by dominant individuals (Metcalfe et al., 1989; McCarthy et al., 1992; Winberg et al., 1993a; Adams and Huntingford, 1996; Adams et al., 1998; MacLean and Metcalfe, 2001). However, subordinate fish do not achieve the growth rates of dominant individuals even when equal rations are consumed (Abbott and Dill, 1989), indicating that factors beyond exclusion from food impact upon the growth of subordinate fish. Sloman et al. (2000c) found that confinement with a conspecific resulted in an increase in the standard metabolic rate of subordinate brown trout (Salmo trutta), and that the magnitude of the increase was correlated with the strength of the social hierarchy within the pair. These findings suggest that there is a metabolic cost associated with low social status. Reductions in hepatic glycogen content (Ejike and Schreck, 1980) and liver condition (where "liver condition" was a composite of hepatic glycogen levels and hepatosomatic index; Sloman et al., 2001b) in subordinate fish, together with increases in plasma glucose levels (Peters et al., 1988; Elofsson et al., 2000), may be indicative of the mobilisation of energy reserves, which could negatively impact growth. Down-regulation of digestive function could also contribute to the lower growth rates of subordinate fish. Chronic subordination in convict cichlid fish resulted in bile retention and consequent hypertrophy of the gall bladder (Earley et al., 2004), a physiological response to low social status that could reduce food conversion efficiency by affecting the capacity to digest food, particularly lipids (Horn, 1998). The occurrence of digestive dysfunction in subordinate salmonids certainly warrants investigation.
Poor condition may also be associated with low social status. Subordinate fish often sustain fin damage from aggressive attacks (nipping) by more dominant individuals (Abbott and Dill, 1985; Abbott et al., 1985; Moutou et al., 1998), and the severity of dorsal fin damage may be correlated with the strength of the social hierarchy (Moutou et al., 1998). Changes in condition factor (where condition factor is calculated from length and weight data) reflect the nutritional or energy status of the fish (Barton et al., 2002), and decreases in condition factor were reported following social interactions resulting in low social status (Sloman et al., 2000a, b). Subordinate trout were found to be more susceptible to bacterial infection than dominant individuals (Peters et al., 1988; Pottinger and Pickering, 1992), a finding that not only reflects the poorer condition of subordinate fish, but is also indicative of links between immune function and social status. Changes in haemopoietic tissues and immune-related cell types consistent with impaired immune function were reported for subordinate rainbow trout (Peters and Schwarzer, 1985; Peters et al., 1988). In addition to increased disease susceptibility, subordinate fish may also display enhanced sensitivity to environmental toxicants such as metals, exhibiting higher uptake rates and greater tissue burdens (Sloman et al., 2002a, 2003b). Interestingly, results contrasting to those for copper and silver were obtained for cadmium, which was found to accumulate to a greater extent in the gill tissue of dominant rather than subordinate fish (Sloman et al., 2003c).
The differences between dominant and subordinate trout in metal uptake may be attributable to the routes through which metals enter the fish; copper and silver utilise sodium transport pathways, whereas cadmium enters the fish via calcium transport pathways (Sloman et al., 2003c). Although little is known of the potential impact of social status on ionic and osmotic regulation in salmonid fish, sodium uptake rates were found to be affected by social status within pairs of rainbow trout, with subordinate fish exhibiting significantly higher uptake rates than dominant individuals (Sloman et al., 2002a, 2003b, 2004). Plasma Na+ concentrations were not affected by social status in either brown trout or rainbow trout (Sloman et al., 2000a, b, 2004), so the higher uptake rates in subordinate fish likely serve to maintain plasma ion concentrations in the face of elevated ion losses via passive efflux across the gills and, to a lesser extent, in the urine (Sloman et al., 2004). The mechanism through which elevated sodium uptake rates in subordinate fish are achieved requires investigation. Increases in the density of branchial ion-transporting chloride cells were reported in sub-dominant fish for brown trout held in small groups (Sloman et al., 2000b), but a direct test of the hypothesis that branchial chloride cell density is affected by social status, using pairs of rainbow trout, failed to find any significant effect (Sloman et al., 2000a). Evaluation of ion-transporting protein (e.g., proton pump, Na+-K+-ATPase) levels and activities might prove useful in this respect.
Data on whether physiological processes such as gas transfer and the maintenance of acid-base balance are affected by social status are also lacking. The elevation of metabolic rate imposed by low social status (Sloman et al., 2000c) might be expected to elicit increases in ventilation volume. In keeping with this prediction, ventilation frequency was found to be slightly, although not significantly, higher over an 11 hr-period in rainbow trout of subordinate social status than in the dominants with which they were confined (Peters et al., 1988). A comprehensive investigation of cardiorespiratory parameters as a function of social status in salmonid fish is certainly needed. Such experiments will, however, be challenging because any differences in ventilation, blood flow, blood gases or acid-base status that are due to social status may be confounded by the invasive techniques required to measure most of these cardiorespiratory parameters.
A physiological response that may act as a visual signal of subordinate social status is skin darkening (O'Connor et al., 1999). Both skin and eye colour darken in salmonid fish that are relegated to low status following social interactions (O'Connor et al., 1999; Höglund et al., 2000, 2002a; Suter and Huntingford, 2002), and in territorial contests between pairs of Atlantic salmon (Salmo salar), initiation of darkening was found to be associated with a decline in aggressive acts directed at the losing fish by the victor (O'Connor et al., 1999). Skin darkness was positively correlated with plasma levels of 
-melanocyte stimulating hormone (-MSH), a pituitary peptide known to elicit chromatophore dispersion as well as increases in chromatophore number (Höglund et al., 2000, 2002a). Like ACTH, -MSH is synthesised from POMC, and while multiple factors are involved in controlling -MSH release from the pituitary, stress-induced increases in the production and release of the POMC-derived peptides may contribute to the darkening of eye and skin colour in subordinate salmonids (Höglund et al., 2000).
Answers to all your Biology Questions
