Katherine A. Sloman

Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss)

SUMMARY Alarm substance is a chemical signal released from fish skin epithelial cells after a predator causes skin damage. When other prey fish detect alarm substance by olfaction, they perform stereotypical predator-avoidance behaviours to decrease predation risk. The objective of this study was to explore the effect of sublethal cadmium (Cd) exposure on the behavioural and physiological responses of juvenile rainbow trout (Oncorhynchus mykiss) to alarm substance. Waterborne exposure to 2 μg Cd l–1 for 7 days eliminated normal antipredator behaviours exhibited in response to alarm substance, whereas exposures of shorter duration or lower concentration had no effect on normal behaviour. Furthermore, dietary exposure to 3 μg Cd g–1 in the food for 7 days, which produced the same whole-body Cd accumulation as waterborne exposure to 2 μg l–1, did not alter normal behaviour, indicating that an effect specific to waterborne exposure alone (i.e. Cd accumulation in the olfactory system) results in behavioural alteration. Whole-body phosphor screen autoradiography of fish exposed to 109Cd demonstrated that Cd deposition in the olfactory system (rosette, nerve and bulb) during waterborne exposure was greater than in all other organs of accumulation except the gill. However, Cd could not be detected in the brain. A short-term elevation in plasma cortisol occurred in response to alarm substance under control conditions. Cd exposures of 2 μg l–1 waterborne and 3 μg g–1 dietary for 7 days both inhibited this plasma cortisol elevation but did not alter baseline cortisol levels. Our results suggest that exposure to waterborne Cd at environmentally realistic levels (2 μg l–1) can disrupt the normal behavioural and physiological responses of fish to alarm substance and can thereby alter predator-avoidance strategies, with potential impacts on aquatic fish communities.

Plasma Cortisol Concentrations Before and After Social Stress in Rainbow Trout and Brown Trout

Two related experiments examined the relationship between plasma cortisol concentrations and the development of social hierarchies in fish. In the first, rainbow trout, Oncorhynchus mykiss, and brown trout, Salmo trutta, were observed for dominance interactions when confined within single‐species pairs for 4, 48, or 168 h. Subordinate members of a pair exhibited significantly higher cortisol concentrations than dominant and single fish, but the pattern of cortisol elevation differed between the two species, being quicker to rise and increasing to a higher level in rainbow trout. Cortisol concentrations were correlated with behavioural measurements; the more subordinate the behaviour exhibited by a fish, the higher its cortisol concentration. Social stress was a chronic stressor, and no acclimation to social status occurred during the week. In the second experiment, measurements of plasma cortisol were made before pairing of rainbow trout and then after 48 h of confinement in pairs. Subordinate fish demonstrated significantly higher concentrations of plasma cortisol both before and after social stress. It therefore appears that in addition to cortisol being elevated during periods of social stress, an association may exist between initial cortisol levels and the likelihood of a fish becoming subordinate.

The effect of social stress on the Standard Metabolic Rate (SMR) of brown trout, Salmo trutta

The effect of social stress, induced by confinement in pairs, on the SMR of the brown trout, Salmo trutta (L.), was investigated. Fish were confined in pairs under laboratory conditions and allowed to establish social hierarchies, with one fish becoming dominant and the other subordinate. The change in SMR of the subordinate fish was significantly greater than that of their respective dominant. Also, the more aggressive the dominant behaved towards the subordinate with which it was paired, the greater the increase in the SMR of the subordinate fish appeared to be. It is concluded that social stress causes an increase in SMR in subordinate fish and therefore imposes a metabolic disadvantage.

Physiological effects of dominance hierarchies within groups of brown trout, Salmo trutta, held under simulated natural conditions

While the existence of dominance hierarchies within natural populations of salmonids is well known, little is known about the physiological consequences of these social interactions. To investigate such physiological effects, replicate groups of four brown trout (Salmo trutta) were held under simulated natural conditions in an artificial stream tank. Behavioural observations allowed the fish to be ranked for dominance. After two weeks, physiological status was assessed through measurements of specific growth rate, condition factor, plasma cortisol and ion concentrations, haematocrit, leucocrit, hepatosomatic index, hepatic glycogen concentration, interrenal cell nuclear area and gill epithelium chloride cell density. Weight gain in the first-ranking (dominant) fish was significantly higher than in the second-ranking fish. In addition, the condition factor of the second-ranking fish decreased over the experimental period while those of the first- and third- ranking fish increased, resulting in significant differences among the three groups. The only other physiological parameter which varied significantly among the ranked fish was chloride cell density, which was significantly higher in the second-ranking fish than in the dominant fish. Cortisol concentrations were low in all fish and did not vary significantly with dominance status. Overall, the least beneficial position, in physiological terms, appears to be the second rank in the dominance hierarchy.

Cadmium affects the social behaviour of rainbow trout, Oncorhynchus mykiss.

The present study investigated both the effects of cadmium on the social interactions of rainbow trout and the differential accumulation of waterborne cadmium among social ranks of fish. Fish exposed to waterborne cadmium concentrations of 2 microg l(-1) for 24 h, followed by a 1, 2 or 3 day depuration period in clean water, had a decreased ability to compete with non-exposed fish. However, the competitive ability of exposed fish given a 5 day depuration period was not significantly impaired. Cadmium accumulated in the olfactory apparatus of fish exposed to waterborne cadmium for 24 h and decreased significantly only after 5 days depuration in clean water. Among groups of ten fish held in stream tanks, where all fish were exposed to cadmium, there were significant effects on social behaviour and growth rate. Dominance hierarchies formed faster among fish exposed to cadmium than among control fish, and overall growth rates were higher in the cadmium treatment. In groups of ten fish, social status also affected tissue accumulation of cadmium during waterborne exposure, with dominant fish accumulating more cadmium at the gill. In conclusion, exposure to low levels of cadmium, affects the social behaviour of fish, in part due to accumulation in the olfactory apparatus, and dominant fish accumulate more gill cadmium than subordinates during chronic waterborne exposure.

Effects of an environmental perturbation on the social behaviour and physiological function of brown trout

We investigated the effect of an environmental perturbation on brown trout, Salmo trutta, dominance hierarchies. Hierarchies were established over a 1-week period under constant simulated natural conditions in artificial stream tanks. In the perturbation treatment water levels were then lowered for a week to simulate a drought, whereas conditions remained the same in the control tanks. We recorded behavioural interactions before and after the environmental perturbation. After the 2-week experiment, we killed the fish and measured growth rate, plasma cortisol, hepatic glycogen content, hepatosomatic index, gill epithelial chloride cell densities and interrenal cell nuclear areas. Aggression showed a nonsignificant increase in the drought tanks when the water level was lowered, and behaviour and social ranking of the fish were significantly affected by the environmental perturbation with a general breakdown in the social hierarchy. The pronounced benefits of dominance in terms of growth rate observed in the control tanks were not apparent in the drought tanks. However, the cortisol concentrations of the drought fish were not significantly higher than those of control fish at the end of the experiment, suggesting that the environmental change itself was not physiologically stressful in the long term. Neither were any other physiological parameters measured significantly different to those of the control tanks. Given that a stable social system (and its physiological consequences) was observed only in a constant environment, misleading conclusions may be drawn if environmental perturbations are not incorporated into experiments studying the behaviour of stream-living fish in simulated natural conditions.

The effects of trace metal exposure on agonistic encounters in juvenile rainbow trout, Oncorhynchus mykiss

The effects of five trace metals, copper, cadmium, nickel, zinc and lead (presented as soluble salts) on the ability of juvenile rainbow trout to form social relationships were investigated. Comparable concentrations of the five metals in relation to their acute 96 h LC50s (concentration at which population mortality=50% at 96 h) were used (i.e. 15% of the 96 h LC50) and water quality parameters (hardness=120 mg l(-1) as CaCO(3), pH 8; DOC=3 mg l(-1)) were kept constant throughout. In the first experiment, trout exposed to sublethal concentrations of cadmium for 24 h displayed significantly lower numbers of aggressive attacks during pair-wise agonistic encounters than fish paired in the copper, nickel, zinc, lead and control water. In a second experiment, fish were exposed to the same concentration of metal for 24 h, and then returned to normal water for 24 h. When these metal pre-exposed fish were paired with non-exposed fish only cadmium pre-exposure had a significant effect on social interaction. All of the cadmium pre-exposed fish became subordinate when paired with non-exposed fish, whereas the probability of a fish pre-exposed to copper, nickel, zinc or lead becoming subordinate did not significantly differ from random. Therefore, at around 15% of the 96 h LC50, different metals exert different effects on the social behaviour of fish, suggesting potential implications for social structure and population stability.

Modulation of catecholamine release and cortisol secretion by social interactions in the rainbow trout, Oncorhynchus mykiss

The objective of the present study was to investigate the effect of social status on the ability of rainbow trout to secrete the stress hormones, cortisol, and catecholamines. Rainbow trout were confined in pairs for six days to permit the formation of dominance hierarchies. An in situ saline-perfused posterior cardinal vein (PCV) preparation was then used to assess cortisol secretion or release of the catecholamine hormones, adrenaline and noradrenaline, in response to the inclusion of appropriate secretagogues in the perfusate. Fish identified as subordinate on the basis of their behaviour showed a characteristic elevation of circulating plasma cortisol concentrations when compared with dominant fish. When the interrenal cells were stimulated in situ with adrenocorticotropic hormone, subordinate fish displayed a significantly lower rate of cortisol secretion than dominant fish. However, social status had no significant effect on either adrenaline or noradrenaline secretion rates upon stimulation of the chromaffin cells in situ with acetylcholine. These results suggest that the chronic elevation of plasma cortisol associated with subordinate social status in rainbow trout reduces the sensitivity of the cortisol-secreting interrenal cells, presumably through negative feedback mechanisms.

Socially-induced changes in sodium regulation affect the uptake of water-borne copper and silver in the rainbow trout, Oncorhynchus mykiss

Subordinate fish take up more copper during water-borne exposure than dominant fish and consequently display higher tissue burdens. The present study demonstrated a similar effect of social status on water-borne silver uptake. We evaluated whether differences in copper and silver accumulation between individuals could be due to differences in metabolic rate, internal concentrations of cortisol or sodium uptake rates. In the absence of social interaction, experimentally increased metabolic rates (via moderate exercise) and elevated whole body cortisol concentrations (via feeding of a cortisol-spiked diet) did not result in increased metal uptake. However, elimination of the difference in sodium uptake rates between dominant and subordinate fish by exposing them to a saturating level of water-borne sodium (50 mM) resulted in an elimination of copper uptake differences. No significant differences in sodium and silver uptake rates were seen between dominant and subordinate fish exposed to elevated silver concentrations. Therefore, it appears that socially-mediated differences in copper and silver accumulation are a result of differences in sodium uptake rates as both silver and copper are known to cross the gill epithelia via sodium transport pathways.

Does Pulsatile Urea Excretion Serve as a Social Signal in the Gulf Toadfish Opsanus beta

This study evaluated the hypothesis that the pulsatile excretion of urea by toadfish could serve as a social signal. In the first experiment, physiological parameters were measured in pairs of dominant and subordinate toadfish. Subordinate toadfish had elevated concentrations of circulating plasma cortisol, an effect maintained even after cannulation. In the second experiment, one fish of a pair was injected with 14C‐urea, and the occurrence of urea pulses during social encounters was documented. Social status did not influence the order of pulsing, that is, whether a dominant or subordinate fish pulsed first during a social encounter. However, in seven out of eight pairs, both toadfish pulsed within 2 h of each other, indicating some form of communication between fish. In the third and final experiment, the response of toadfish to urea (natural or synthetic) was observed. There was a tendency for toadfish to avoid synthetic urea but there was no apparent behavioural response to water containing toadfish urea. Pulsing events do not appear to play an integral role during social encounters as previously hypothesised, but the close timing of pulses in toadfish pairs suggests some transfer of information.