Physiological Causes and Consequences of Social Status in Salmonid Fish1

Physiological Causes and Consequences of Social Status in Salmonid Fish1

Gilmour, Kathleen M

SYNOPSIS.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.

INTRODUCTION

Salmonid fish readily form dominance hierarchies in the wild or under laboratory conditions (e.g., Kalleberg, 1958; Noakes and Leatherland, 1977; Bachman, 1984; Nakano, 1995; Adams et al., 1998). These “pecking order” social structures are established through agonistic interactions, with each fish being ranked according to its ability to out-compete other individuals within the group (Metcalfe et al., 1989; Adams et al., 1998). Typically, dominant fish are able to monopolise essential but limited resources, such as food or shelter, while subordinate fish may be excluded from such resources and consequently suffer penalties such as increased mortality (McCarthy et al., 1992; Elliott, 1994; Kadri et al., 1996). Behavioural correlates of dominant social status are well characterised and include possession of choice positions within the environment, acquisition of a larger share of the available food, and aggression directed at fish of lower social status (Fausch, 1984; Abbott and Dill, 1985; Abbott et al., 1985; Metcalfe, 1986; Metcalfe et al., 1989; Huntingford et al., 1990; McCarthy et al., 1992; Sloman et al., 20006). Subordinate fish, by contrast, often exhibit behavioural inhibition including reductions in (or the absence of) activity, feeding, and aggression (Abbott and Dill, 1985; McCarthy et al., 1992; Winberg et al., 1993e; Moutou et al., 1998; Øverli et al., 1998). Because social status is of demonstrable significance to individual performance (Ryer and Olla, 1996; Adams et al., 1998; Metcalfe, 1998; Petersson et al., 1999; Höjesjö et al., 2002), aggressive interactions and the resultant dominance hierarchies in salmonid fish have been the subject of considerable research. Behavioural aspects of social hierarchies have been well documented, and more recently, attention has been focused on the impact of social interactions on brain monoaminergic activity as the underlying basis for the behavioural differences between fish of high and low social status (reviewed by Winberg and Nilsson, 1993). The physiological consequences of social status are less well characterised (reviewed by Sloman and Armstrong, 2002), however, as is the potential for physiological factors to influence the outcome of social interactions. Indeed, whether measurable physiological consequences of social status exist within natural populations of salmonid fish remains unclear. Such interactions between physiology and social status in salmonid fish are the focus of the present paper. Particular emphasis is placed on the role played by cortisol, the principle corticosteroid stress hormone in salmonid fish. Discussion is directed to the hypothesis that many of the negative physiological changes associated with low social status can be attributed to high circulating cortisol levels. Additionally, the possibility that circulating cortisol levels may influence the outcome of agonistic interactions is raised.

SUBORDINATE SOCIAL STATUS AS A CHRONIC STRESS

Evidence that subordinate social status constitutes a chronic stress in salmonid fish has been obtained from measurements of circulating cortisol levels. Activation of the hypothalamo-pituitary-interrenal (HPI) axis resulting in mobilisation of the corticosteroid hormone cortisol (Mommsen et al., 1999), together with release of the catecholamine hormones (adrenaline and noradrenaline) via the sympathetico-chromaffin pathway (Reid et al., 1998), constitute the primary neuroendocrine response of fish to stress (Barton and Iwama, 1991; Pickering and Pottinger, 1995; Sumpter, 1997; Wendelaar Bonga, 1997). Circulating catecholamine responses to social interactions in fish have not been investigated as cannulation of the fish is necessary to assess plasma catecholamine levels, which increase essentially immediately upon exposure to stressors, including handling to sample blood (Reid et al., 1998). Prolonged elevation of plasma cortisol levels is frequently used as a marker for exposure to a chronic stressor, with the magnitude of the cortisol response generally reflecting the severity of the stressor (Pickering and Pottinger, 1995; Wendelaar Bonga, 1997).

In salmonid fish confined in pairs, subordinate individuals characteristically exhibit elevated plasma cortisol levels (Laidley and Leatherland, 1988; Pottinger and Pickering, 1992; Øverli et al., 1999a; Elofsson et al., 2000; Sloman et al., 2000a, 2001a, 2002a; Pottinger and Carrick, 2001; Hoglund et al., 2002a), and the magnitude of the rise in plasma cortisol may be correlated with the strength of the social hierarchy (Sloman et al., 2001a). Cortisol responses to the formation of social hierarchies within small groups of salmonid fish appear to be more variable, with some studies reporting elevated cortisol levels in subordinate fish (Ejike and Schreck, 1980; Winberg and Lepage, 1998; Hoglund et al., 2000), but not others (Pottinger and Pickering, 1992; Øverli et al., 1999b; Sloman et al, 2000b, 2001b, 2002c). Differences in group size or environment as well as species differences in aggressiveness could all contribute to this variability. While plasma cortisol increases rapidly (within 5 min) with the onset of agonistic interactions in both fish within a pair, cortisol concentrations in fish that subsequently achieve dominant status soon return to resting levels (within 3 hr a time frame that typically accords well with cessation of most overt aggression; Øverli et al., 1999a), whereas elevation of plasma cortisol in subordinate fish may be prolonged for 24 hr to 7 days or more (Øverli et al., 1999a; Sloman et al., 2001a) and therefore social subordination may be viewed as a chronic stressor.

Circulating cortisol concentrations reflect the balance between production and clearance of the hormone, where production is the combined result of cellular biosynthesis and secretion into the blood, and clearance is the rate at which the hormone is removed from the blood (Mommsen et al., 1999). Of these three parameters, namely biosynthesis, secretion and clearance, only cortisol secretion has been investigated to any significant extent as a function of social status in salmonid fish. The biosynthesis and metabolic clearance of cortisol were reviewed by Mommsen et al. (1999), who pointed out the need for additional studies to investigate the environmental regulation of cortisol biosynthesis, a need that clearly applies with respect to the potential impact of social status on these processes. Cortisol secretion into the circulation is controlled by the hypothalamic neuropeptide corticotropin-releasing factor (CRF), which stimulates the release of adrenocorticotropic hormone (ACTH) from the anterior pituitary and ACTH, in turn, acts on the interrenal cells to elicit cortisol secretion (reviewed by Wendelaar Bonga, 1997; Mommsen et al., 1999). Secretion via this pathway may be modulated by the negative feedback actions of cortisol at the levels of the hypothalamus and pituitary (Mommsen et al., 1999).

The maintenance of high circulating cortisol levels in subordinate individuals reflects chronic activation of the HPI axis. Socially subordinate salmonids exhibit elevated CRF mRNA expression in the preoptic area of the brain (Doyon et al., 2003), up-regulation of mRNA expression of the ACTH precursor pro-opiomelanocortin (POMC) in the pituitary (Winberg and Lepage, 1998), and plasma ACTH concentrations that are significantly greater than those in dominant individuals (Hoglund et al., 2000). These differences in CRF, POMC and ACTH were documented for various periods of social interactions ranging from 1 to 7 days (Winberg and Lepage, 1998; Hoglund et al., 2000; Doyon et al., 2003), supporting the chronic nature of HPI axis activation in low ranking individuals. Also in accordance with chronic HPI axis activation, changes consistent with greater synthetic activity were documented for both the ACTH-producing cells of the pituitary (Boddingius, 1976) and the interrenal cells of subordinate rainbow trout (Oncorhynchus mykiss) after 14-17 days of social interactions (Boddingius, 1976; Noakes and Leatherland, 1977). However, basal (unstimulated) cortisol secretion rates for interrenal tissue preparations did not differ significantly between dominant and subordinate rainbow trout (Sloman et al., 2002e), suggesting low social status affects primarily the regulatory pathways for cortisol secretion rather than up-regulating cortisol synthesis or secretion by the interrenal cells directly.

Although CRF and ACTH constitute the primary pathway for controlling cortisol secretion, other neural and/or hormonal pathways could potentially contribute to maintaining activation of the HPI axis in subordinate salmonid fish. Several neuropeptides, including urotensin-I, possess ACTH-releasing abilities (Lederis et al., 1994), while cortisol secretion from the interrenal cells can be stimulated or modulated by a variety of hormones and neuropeptides, including α-melanophore stimulating hormone, growth hormone, and urotensin I (Sumpter, 1997; Wendelaar Bonga, 1997; Mommsen et al., 1999). Of particular interest is the possible role played by the monoamine neurotransmitter serotonin. Brain serotonergic activity is increased by social subordination in salmonid fish (Winberg and Nilsson, 1993), and several lines of evidence suggest that hypothalamic serotonin could be involved in regulating the HPI axis. This evidence includes the significant correlation reported between hypothalamic serotonergic activity and plasma cortisol (Winberg and Lepage, 1998; Øverli et al, 1999a) or ACTH levels (Höglund et al., 2000) in subordinate rainbow trout, the dose-dependent changes in circulating cortisol elicited by systemic administration of a serotonin receptor agonist (Winberg et al., 1997; Höglund et al., 2002e), and the modulation of stress-induced rises in circulating cortisol with dietary tryptophan supplementation; tryptophan is the precursor of serotonin (Lepage et al., 2002, 2003). Overall, however, very little is known of the extent to which factors beyond CRF and ACTH contribute to the sustained elevation of circulating cortisol levels in subordinate salmonid fish.

Chronic activation of the HPI axis, in turn, appears to dampen the sensitivity of the cortisol response to additional, acute stressors in subordinate fish. For example, Øverli et al. (1999b) found that only Arctic charr (Salvelinus alpinus) ranked as dominant were able to increase plasma cortisol significantly following a handling stress. This modulation of the cortisol response reflects, at least in part, reduced interrenal tissue sensitivity to ACTH stimulation in subordinate fish (Sloman et al., 2002b), and is in keeping with a general trend towards desensitisation of the cortisol response in fish that are chronically stressed by a wide array of factors, including high stocking density, confinement, poor water quality or pollutants (reviewed by Wendelaar Bonga, 1997; Mommsen et al., 1999). Less is known of the potential for chronic stress, and particularly chronic behavioural stress, to impact upon the adrenergic stress response. The literature in this area (see review by Reid et al., 1998) suggests that chronic stress entailing repeated mobilisation of catecholamines leads to desensitisation of the catecholamine release pathway (Reid et al., 1994; Perry et al., 1996), whereas elevation of plasma cortisol levels in the absence of significant catecholamine release may enhance the responsiveness of the chromaffin cells (Reid et al, 1996; Montpetit and Perry, 1998). Either or both of these situations may apply to social interactions; bouts of agonistic interactions could be envisaged as causing repeated catecholamine release, while prolonged elevation of plasma cortisol levels occurs in subordinate fish. Although neither catecholamine storage levels (J. Thomas and K. M. Gilmour, unpublished observations) nor the in vitro sensitivity of catecholamine release to a secretagogue (Sloman et al., 2002b) were found to differ between dominant and subordinate rainbow trout, whether catecholamine mobilisation in vivo in response to an acute stressor is affected by social status remains to be ascertained.

Finally, there may be physiological consequences of low social status associated with the stress hormone profile characteristic of subordinate fish. The catecholamine hormones initiate numerous effects that serve primarily to modulate cardiorespiratory function and mobilise energy reserves in preparation for a “fight-or-flight”-type response (Pickering and Pottinger, 1995; Wendelaar Bonga, 1997; Reid et al., 1998). High cortisol or catecholamine levels appear to impinge upon several of these effects, most notably the red blood cell adrenergic response (Perry and Reid, 1993; Gilmour et al., 1994; Perry et al., 1996). In rainbow trout, preliminary data suggest that low social status neither compromises (as might be expected from high catecholamine levels) nor pre-adapts (as might be expected from high cortisol levels) the red blood cell adrenergic response (J. Thomas and K. M. Gilmour, unpublished observations). However, additional investigation of the impact of social status on catecholamine responses is needed. Cortisol plays important roles in metabolism, ionic and osmotic regulation, and immune function under normal conditions as well as during periods of stress (Wendelaar Bonga, 1997; Mommsen et al, 1999). Transient elevations of circulating cortisol levels elicited by acute stressors are undoubtedly beneficial, but an increasing body of evidence suggests that long-term elevation of plasma cortisol is associated with detrimental physiological consequences (Pickering and Pottinger, 1995; Wendelaar Bonga, 1997; Mommsen et al, 1999). Because the influence of cortisol is so wide-reaching, the physiological consequences of low social status in salmonid fish will be outlined prior to discussing the extent to which these consequences can be attributed to sustained high cortisol levels.

PHYSIOLOGICAL CONSEQUENCES OF SOCIAL STATUS

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., 2003e). 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 ai, 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 iontransporting 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 α-melanocyte stimulating hormone (α-MSH), a pituitary peptide known to elicit chromatophore dispersion as well as increases in chromatophore number (Höglund et al, 2000, 2002a). Like ACTH, α-MSH is synthesised from POMC, and while multiple factors are involved in controlling α-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).

INTERACTIONS BETWEEN CORTISOL AND SOCIAL STATUS

To what extent the detrimental physiological consequences of low social status stem from the chronic elevation of circulating cortisol levels is unclear at present (Fig. 1). Certainly, effects similar to those observed in salmonid fish of low social status have been documented in fish exposed to a variety of chronic stressors such as poor water quality or pollutants (Wendelaar Bonga, 1997), as well as following long-term experimental elevation of plasma cortisol concentrations. Cortisol levels have been manipulated experimentally either using intraperitoneal implants that slowly release cortisol into the circulation, or by feeding fish cortisol-spiked food. In either case, the growth of salmonid fish is depressed by cortisol treatment (Barton et al, 1987; Gregory and Wood, 1999; De Boeck et al, 2001). Cortisol-induced appetite suppression (Barton et al., 1987; Gregory and Wood, 1999), mobilisation of energy reserves as evidenced by increased plasma glucose concentrations (Barton et al, 1987; Morgan and Iwama, 1996; De Boeck et al., 2001) and reduced hepatic glycogen levels (Barton et al., 1987), morphological alterations to the digestive tract (Barton et al., 1987), reduced food conversion efficiency (Gregory and Wood, 1999), and increased metabolic rate (Morgan and Iwama, 1996; De Boeck et al., 2001), may all contribute to the lower growth rates of cortisol-treated fish. In addition to lowering growth rate, exogenous cortisol administration decreases condition factor (Barton et al., 1987; Gregory and Wood, 1999), and cortisol-treated rainbow trout exhibited significantly more fin damage than their untreated conspecifics when held in mixed groups (Gregory and Wood, 1999). Increased mortality accompanies cortisol treatment (Pickering and Pottinger, 1989; Gregory and Wood, 1999), and reflects enhanced susceptibility to common bacterial and fungal diseases (Pickering and Pottinger, 1989), presumably as a result of changes in immune cell numbers and function (Barton et al., 1987). In short, the physiological decline associated with low social status in salmonid fish likely is the outcome, to a significant extent, of the chronic elevation of circulating cortisol levels. In preliminary experiments carried out to test this hypothesis, the reductions in specific growth rate and condition factor normally associated with subordinate social status were partly prevented by treatment of rainbow trout with the glucocorticoid receptor blocker RU486 prior to pairing with a size-matched conspecific (Fig. 2).

While both behaviour (e.g., exclusion from food, fin nipping) and secondary effects of high long-term cortisol levels contribute to the negative physiological consequences experienced by low-ranking salmonid fish, direct responses to social stress itself are also likely (Barton, 2002). Even within social hierarchies where all fish exhibit similar plasma cortisol concentrations, subordinate fish may still accrue significant physiological disadvantages (Pottinger and Pickering, 1992; Sloman et al., 2000b, 2001b, 2002c). Furthermore, some physiological consequences of low social status seem to be inconsistent with raised cortisol concentrations; an example is the greater passive Na+ efflux across the gills of subordinate rainbow trout (Sloman et al, 2004), when cortisol, at least in vitro, appears to promote epithelial tightness (Wood et al., 2002; Zhou et al, 2003). The lack of complete alleviation by RU486 treatment of the reductions in growth and condition factor associated with low social status is also indicative of direct responses to social stress (Fig. 2). Moreover, differences in interrenal cell sensitivity to ACTH in rainbow trout have been detected between confinement stress (resulting in endogenous cortisol mobilisation) and exogenous cortisol administration (Balm and Pottinger, 1995). Central responses to stress in fish are not yet well characterised, but the available evidence suggests that stress effects may be exerted on a wide array of brain neurotransmitters, neuroendocrine peptides, and pituitary hormones (Sumpter, 1997; Wendelaar Bonga, 1997). Social stress-induced changes in brain monoaminergic activity are among the best documented central responses to stress, but even here, data on the downstream effects of these changes remain sparse (Winberg and Nilsson, 1993; Summers, 2002). Clearly, this area is one that merits further attention.

PHYSIOLOGICAL DETERMINANTS OF SOCIAL STATUS?

While the physiological hallmarks of subordination in salmonid fish become apparent soon after social interactions are initiated, the potential for physiological status to influence the outcome of social encounters remains an intriguing possibility about which little is known. Competitive ability is a key determinant of the winner of an agonistic contest, although factors such as prior residence (Huntingford and Garcia de Leaniz, 1997; Rhodes and Quinn, 1998; Cults et al., 1999a, b) and environmental conditions (water levels and/or flow rates; Sloman et al., 2001b, 2002c, waterborne metals; Sloman et al., 2003a, c) also influence the end result of social interactions (Fig. 3). How competitive ability is assessed by individual fish during a contest remains unclear. Relative size may be used as a signal, at least in some salmonid species. A weight advantage of as little as 5% ensured dominance to the heavier fish in pairwise contests between naïve rainbow trout (Abbott et al., 1985), while a length difference of 6% in coho salmon (Oncorhynchus kisutch) parr was sufficient to overcome the advantage conferred by prior residence (Rhodes and Quinn, 1998; see also Holtby et al, 1993). Larger body size was also a predictor of victory in brown trout fry competing for territories (Johnsson et al., 1999). By contrast, no relationship was found between size and eventual social status in juvenile Atlantic salmon, Arctic charr, or masu salmon (Oncorhynchus masou) (Huntingford et al., 1990; Adams and Huntingford, 1996; Yamamoto et al, 1998). Substantial size asymmetries (> 12% length difference), however, may result in dominant status for the larger individual even in species where size is not a reliable indicator of dominance (Cutts et al., 1999b). Olfactory cues may also be important in evaluating competitive ability. Both aggression and competitive success in rainbow trout were significantly reduced by exposure to waterborne cadmium (Sloman et al., 2003a, c). The effect of cadmium on social status was attributed to impaired olfactory capacity resulting from cadmium accumulation in the olfactory rosette, since normal competitive ability during recovery from cadmium exposure was regained at a time when cadmium levels in the olfactory rosette had declined (Sloman et al., 2003c). Interestingly, there is evidence for chemical communication of “stress” (where stress is indicated by high circulating cortisol levels) in fish (Olivotto et al., 2002), which might also contribute to signalling during social encounters, although a recent study found no evidence that juvenile Arctic charr differentiated between dominant and subordinate siblings on the basis of odour (Olsen et al, 2003).

The competitive ability of an individual fish is likely to be governed by numerous factors (Fig. 3), including innate aggressiveness (Holtby et al., 1993; Adams and Huntingford, 1996; Adams et al, 1998; Cutts et al, 1999a) and feeding motivation (Johnsson et al., 1996). Prior social experience also affects competitive ability in subsequent contests (Abbott et al., 1985; Rhodes and Quinn, 1998; Johnsson et al, 1999), probably because of the changes in brain monoaminergic activity induced by winning or losing (Winberg and Nilsson, 1993), and the impact of these changes on aggressive behaviour (Winberg and Nilsson, 1993; Øverli et al., 1999a; Höglund et al, 2001; Winberg et al, 2001). For example, dominant social status was effectively assured by experimental elevation of brain dopaminergic activity (Winberg and Nilsson, 1992). Physiological status would also be expected to be important in determining competitive ability, with the prediction being that parameters such as abundant energy reserves, good condition and perhaps high metabolic capacity would correlate with competitive strength. At least three lines of evidence support the contention that the outcome of social interactions can be influenced by physiological disparities. First, salmonids with higher metabolic rates (prior to social interactions) tend to achieve higher social status (Metcalfe et al., 1995; Yamamoto et al, 1998; Cutts et al, 1999b; McCarthy, 2001). High metabolic rate is correlated with greater aggression levels in juvenile Atlantic salmon (Cutts et al, 1998), providing a mechanism through which high metabolic rate can translate into competitive success. The correlation between resting metabolic rate and social standing among individuals is distinct from the change (increase) in metabolic rate that accompanies relegation to subordinate status within an individual. Second, the likelihood of attaining dominant status can be significantly enhanced by growth hormone treatment in juvenile rainbow trout (Johnsson and Björnsson, 1994). Growth hormone treatment does not affect social status directly, but rather appears to increase aggressive behaviour and feeding motivation (Jönsson et al., 1998); whether these behavioural changes reflect central nervous system actions of growth hormone or are secondary to metabolic effects induced by the hormone remains to be resolved (Jönsson et al., 2003). Finally, social status appears to be affected by circulating cortisol levels. Gregory and Wood (1999) found that cortisol-treated fish suffered significantly more fin damage than did their untreated tankmates when held in mixed groups, suggesting that elevated plasma cortisol put the treated fish at a competitive disadvantage. More purposefully, measurements of cortisol concentrations in rainbow trout both before and after 48 hr of confinement in pairs revealed that plasma cortisol prior to social interactions was significantly higher in the rainbow trout that were subsequently categorised as subordinate than in those that achieved dominance (Sloman et al., 2001a). Preliminary data from a direct test of the hypothesis that high cortisol levels pre-dispose salmonid fish to low social status indicated that cortisol treatment countered the effect of large size in determining dominance within pairs of rainbow trout (Fig. 4). Whereas the larger trout became dominant in 86% of pairs in which both fish were untreated, the same was true of only 40% of pairs in which the large fish received an intraperitoneal implant to elevate plasma cortisol concentrations; chisquare analysis revealed that size had a significant effect on social status within the control group (X^sup 2^ = 11.57, P

The mechanism(s) through which high circulating cortisol levels affect the outcome of social interactions requires investigation. One possibility is that the depression of physiological condition attendant upon chronic cortisol elevation (see above) diminishes competitive ability. Alternatively, cortisol may influence behaviour directly or indirectly, a possibility that is attractive given that even 48 hr of cortisol treatment prior to pairing had an impact on the outcome of social interactions in rainbow trout (Fig. 4). Cortisol receptors are widely distributed in the forebrain of the rainbow trout, with particular concentration in the hypothalamus and preoptic regions (Allison and Omeljaniuk, 1998; Teitsma et al, 1998), providing for a neuromodulatory role of cortisol on behaviour. Recent work on rainbow trout supports an indirect role for cortisol in modifying behaviour. Experimental elevation of plasma cortisol for ~ 1 hr was sufficient to significantly enhance the locomotory response to an intruder, while longer-term cortisol treatment (48 hr) inhibited both aggressive behaviour and activity in an intruder test (Øverli et al., 2002a). The effects of cortisol were deemed to be indirect because locomotor activity in the absence of an intruder was unchanged (Øverli et al., 2002a). The reduced appetite of cortisol-treated rainbow trout reported by Gregory and Wood (1999), which may be mediated through hormone-induced changes in metabolism or feeding motivation, is also consistent with an indirect effect of cortisol on (feeding) behaviour, although a direct effect cannot be ruled out. In a model system that is likely to prove useful for the studies necessary to elucidate the complex linkages among stress responses, behaviour, and central nervous or neuroendocrine systems, rainbow trout bred to exhibit low responsiveness to confinement stress were dominant in paired encounters over conspecifics from a line selected for high responsiveness (Pottinger and Carrick, 2001). Circulating cortisol concentrations in the absence of stress did not differ between the two lines, suggesting that the cortisol response to the onset of agonistic interactions (Øverli et al, 1999a) influences their outcome, and/or that behavioural characteristics associated with stress responsiveness (perhaps implemented through brain monoaminergic systems; Øverli et al., 2001) are also important in determining competitive ability (Pottinger and Carrick, 2001; Øverli et al, 2002b). The possible interplay between cortisol and brain monoaminergic systems with respect to the control of behaviour is of particular interest. There is evidence to support the involvement of brain monoaminergic systems in the control of the HPI axis and stress responses (see above). Whether a reciprocal association exists, i.e. whether circulating cortisol levels can impinge on brain monoaminergic activity, is unknown. If present, however, changes in aggressive behaviour modulated by cortisol-induced alteration of central monoaminergic activity could provide a mechanism through which social status is influenced by circulating cortisol concentrations.

CONCLUSIONS

Dominance hierarchies in salmonid fish provide a valuable paradigm with which to study the intimate linkages between behaviour and physiology. The social standing of an individual fish is both influenced by its underlying physiological status, which is implicated in determining competitive ability, and important in establishing its physiological status, with low-ranking individuals experiencing physiological decline. These relationships appear to be governed by multifaceted interactions among behaviour (particularly aggression), neural and endocrine systems, and stress responses. The brain serotonergic system and the corticosteroid stress hormone cortisol, as key players in the associations between social behaviour and physiology, will be central to future investigations aimed at fully elucidating the physiological causes and consequences of social status in salmonid fish.

ACKNOWLEDGMENTS

Thanks are extended to Dr. G. A. Bartholomew, the Society for Integrative and Comparative Biology, and the symposium organisers, Dr. R. B. Huey and Dr. G. E. Hofmann. Dr. K. A. Sloman is thanked for access to unpublished work, and Dr. S. F. Perry is gratefully acknowledged for comments on the manuscript. JBT was supported by an NSERC of Canada post-graduate scholarship, while financial support for JDD was provided by the PREA program. Original research reported here was funded by NSERC, CFI and OIT grants to KMG.

1 From the Symposium Integrative Biology: A Symposium Honoring George A. Bartholomew presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5-9 January 2004, at New Orleans, Louisiana

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KATHLEEN M. GILMOUR,2,3 JOSEPH D. DIBATTISTA,3 AND JUSTIN B. THOMAS3

Department of Biology, Carleton University, Ottawa, ON K1S 5B6, Canada

2 E-mail: katie.gilmour@science.uottawa.ca

3 Present address for all authors: Department of Biology, University of Ottawa, 150 Louis Pasteur, Ottawa, Ontario KlN 6N5, Canada.

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