C. J. CUTTS,* N. B. METCALFE and A. C. TAYLOR

Transcription

1 Functional Ecology 2002 Juvenile Atlantic Salmon (Salmo salar) with relatively Blackwell Science Ltd high standard metabolic rates have small metabolic scopes C. J. CUTTS,* N. B. METCALFE and A. C. TAYLOR Fish Biology Group, Division of Environmental & Evolutionary Biology, Graham Kerr Building, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK Summary 1. There is an established relationship between metabolism and behavioural dominance in several fish species, such that individuals with higher standard metabolic rates tend to be more dominant. It has also been suggested that metabolic scope increases with standard metabolic rate. 2. Energetically expensive behaviours attributable to dominance, such as aggression, can be carried out to a greater extent within larger metabolic scopes. This study therefore tests the hypothesis that juvenile salmon with higher standard metabolic rates (which tend to be dominant) have larger metabolic scopes. 3. It was found that salmon with high standard metabolic rates (corrected for body mass) in fact had smaller metabolic scopes than conspecifics with relatively low standard metabolic rates. Possible reasons for their potential dominance while having small metabolic scopes and high relative standard metabolic rates are discussed. Key-words: Aggression, dominance, energetics, metabolism, resource allocation Functional Ecology (2002) Ecological Society Introduction Standard metabolic rate (SMR) is the minimal maintenance or resting metabolic rate of unfed animals, below which physiological function is impaired (Brett & Groves 1979; Priede 1985). Recent studies have shown a link between metabolism and behavioural dominance in several fish species: Spinyhead and Roughhead Blennies, Acanthemblemaria spinosa and A. aspera (Clarke 1992); Atlantic Salmon, Salmo salar (Metcalfe, Taylor & Thorpe 1995; Cutts, Metcalfe & Taylor 1998, 1999a), Masu Salmon, Oncorhynchus masou (Yamamoto, Ueda & Higashi 1998) and Arctic Charr, Salvelinus alpinus (Cutts, Adams & Campbell 2001). Metcalfe et al. (1995) showed that fish with higher relative standard metabolic rates are more dominant in pairwise contests, and hypothesized that the greater standard metabolic rate was a consequence of a greater metabolic scope (Priede 1985) within which behaviours attributable to dominance (e.g. aggression) could be performed at a greater intensity. Cutts et al. (1998) demonstrated that juvenile salmon with high standard metabolic rates were indeed more aggressive, and that dominance was probably mediated through greater aggression. However, the relationship between standard Author to whom correspondence should be addressed. C-Cutts@seafish.co.uk *Present address: Seafish Marine Farming Unit, Ardtoe, Acharacle, Argyll PH36 4LD, UK. metabolic rate and metabolic scope was untested in that study. SMR can be measured either directly with unfed, inactive fish (e.g. Edwards et al. 1970; Soofiani & Hawkins 1982) or by extrapolating measurements in active fish back to zero activity (e.g. Brett 1964; Lucas & Priede 1992). Ordinarily, fish live above this resting level owing to activities such as feeding and locomotion, and the typical rate of metabolism that they experience is termed routine metabolic rate. However, there is an upper limit on aerobic metabolic rate termed the active metabolic rate (AMR). The difference between active and standard metabolic rate is termed the metabolic scope (Fry 1947) and the animal must function within its confines. Metabolic scope can either be expressed as the absolute difference between the two limits (in ml O 2 g 1 h 1, e.g. Wieser 1985; Wieser & Medgyesy 1990), or as a metabolic expansivity coefficient (AMR/ SMR, e.g. Lucas & Priede 1992), also known as factorial metabolic scope (FMS; Wieser & Forstner 1986; Armstrong, Priede & Lucas 1992). Both the standard and active metabolic rates of healthy fish are mandatory and it has been assumed that healthy, postabsorptive fish cannot regulate their magnitude (Priede 1985), although starvation and stress can lower and raise SMR, respectively (O Connor, Taylor & Metcalfe 2000; Sloman et al. 2000). Hayes, Garland & Dohm (1992) hypothesized that any correlation between metabolic rate and life history (e.g. behavioural dominance) arose from consequences 73

2 74 C. J. Cutts et al. of resource allocation. The principle of resource allocation states that available energy is partitioned between maintenance, growth and reproduction (Gadgil & Bossert 1970). This would manifest itself as variation in, e.g., mammalian litter size (a life-history variable) correlating with variation in costs of maintenance (measured as basal metabolic rate). In fish, the principle of resource allocation is analogous to the partitioning of components of metabolism such as locomotor activity and feeding metabolism within the limits of standard and active metabolic rate (Brett & Groves 1979; Priede 1985). Feeding metabolism is associated with gut motility, digestive processes and postfeeding activity, and was described by Beamish (1974) as apparent specific dynamic action (SDA). Metabolic rate is usually elevated (because of SDA) for some hours following feeding (Elliott 1976; Vahl & Davenport 1979). Locomotor metabolism can also account for a large proportion of the metabolic scope, so in fish there is a continual conflict between locomotion and feeding. For example, in Largemouth Bass (Micropterus salmoides; Tandler & Beamish 1981) and juvenile Cod (Gadus morhua; Soofiani & Priede 1985), feeding metabolism can occupy all the metabolic scope, theoretically allowing none for locomotion within the confines of aerobic metabolism. Therefore fish may have a potential power budgeting problem, especially when foraging (Brett & Groves 1979; Priede 1985), and so the greater their metabolic scope, the less their behaviour will be constrained. Much attention has been given to the allometric scaling of standard and active metabolic rate with mass. Standard metabolic rate (measured as oxygen consumption per gram) generally scales with size with a mass exponent of less than unity (<1), implying that heavier fish respire less on a per gram basis, whereas active metabolic rate usually scales with size with a mass exponent of greater than unity (>1), implying that heavier fish have higher active metabolic rates on a per gram basis. Consequently, the metabolic scope usually increases with fish size (Goolish 1991; Armstrong et al. 1992). However, little is known about how individual deviations from allometric predictions of standard metabolic rate affect deviations from predictions of active metabolic rate, after controlling for body size. Deviations from predicted metabolic rate are measured as residuals (the difference between metabolic rate predicted on the basis of body mass and the actual metabolic rate). This method of investigating intraspecific variation in metabolic rate has been advocated across a wide range of taxa: mammals (McNab 1988), birds (Daan, Masman & Groenewold 1990) and, more recently, fish (Metcalfe et al. 1995; Cutts et al. 1999a; O Connor et al. 2000). The relative metabolic rates of fish have been shown to be consistent over long time periods, with some individuals consistently having a higher metabolic rate for their size than others (McCarthy 2000; Cutts et al. 2001). Metcalfe et al. (1995) hypothesized that fish with high standard metabolic rates (after correcting for body size) were dominant through greater aggression, mediated via a correspondingly large metabolic scope. The large metabolic scope would allow them to carry out costly acts of aggression. Using the same techniques of residual analysis, the present study tested the hypothesis that juvenile Atlantic Salmon (Salmo salar L.) with high standard metabolic rates (after controlling for size) also have correspondingly high metabolic scopes. Metabolic scope in individual fish was measured as an expansivity coefficient, and related to the standard metabolic rate of the individual fish. The implications for resource allocation in juvenile salmon are discussed, given that salmon with high standard metabolic rates tend to be more aggressive. Materials and methods SOURCE AND MAINTENANCE OF FISH All fish used in this study were underyearling offspring of sea-run adults from the River Almond, Perthshire, UK, and were reared at the SERAD Almondbank hatchery prior to removal to the University Field Station, Rowardennan, Loch Lomond, UK. Prior to experiments, all fish were kept in tangential flow hatchery tanks at ambient temperature and photoperiod and fed ad libitum with commercial pelleted food (BOCM Pauls, Renfrew, UK). GENERAL RESPIROMETRY METHODS Metabolic rates of juvenile salmon were measured as oxygen consumption rates by placing individual fish in Perspex respirometry chambers through which water continually flowed at a known rate. Water temperature was noted in order to estimate the capacitance of oxygen in the water (βwo 2, ml O 2 l 1 ) during a series of oxygen consumption measurements, and was kept constant throughout each trial. The water was kept fully oxygensaturated by means of an air-stone in the header tank, and flowed by gravity from the header tank through the respirometry chambers. A rack of 20 such chambers allowed the oxygen consumption rates of 20 salmon to be measured per day. The oxygen saturation of the water flowing into and out of the respirometer chamber was measured using a microcathode oxygen electrode contained within a thermostatted chamber and connected to an oxygen meter (Strathkelvin Instruments, Glasgow, UK). The electrode was calibrated prior to use against aerated water (at the same temperature) and against a solution having an oxygen saturation of zero (sodium sulphite in 0 01 M sodium tetraborate). Water samples from the inflow and outflow water were injected in turn into the chamber containing the electrode and the percentage oxygen saturation of the water determined. Following the conversion of the oxygen saturation values into

3 75 Metabolic scope in juvenile salmon oxygen concentrations using the tables in Steffensen (1989), the rates of oxygen consumption (VO 2, ml O 2 h 1 ) were calculated using the equation: VO 2 = V W C W O 2 eqn 1 where V W is the flow rate of water through the respirometry chamber (l h 1 ; measured by collecting the water outflow from each tube in a beaker over a measured time period [a minimum of 2 min] and weighing it) and C W O 2 is the difference in the oxygen concentration between the inflow and outflow water ([%reduction/100]βwo 2, ml O 2 l 1 ; where βwo 2 is the capacitance of oxygen in the water; Steffensen 1989). For a fuller account of the respirometry methodology, see Cutts et al. (1998). MEASURING AMR, SMR AND METABOLIC SCOPE In order to measure AMR, fish were transferred from a holding tank where they had been fed ad libitum and put in a 20-l bucket. Their routine metabolic rates would have already been elevated by the specific dynamic action (SDA) resulting from feeding (Beamish 1974; Brett & Groves 1979; Priede 1985). The fish were agitated into burst swimming performance while in the bucket by being chased with a hand-net for a maximum of 5 min. They were then netted and immediately placed in the respirometry chambers. This is thought to induce active metabolic rate; moving from a stationary position to a burst swimming speed is energetically very inefficient (Dickson & Kramer 1971) and oxygen consumption during aerobic recovery after exercise is known to be higher than that observed during exercise (Soofiani & Priede 1985). Moreover, chasing protocols have been thought to be biochemically and physiologically analogous to exhaustive exercise (Wieser, Platzer & Hinterleitner 1985; Pearson, Spriet & Stevens 1990; Reidy et al. 1995). The first metabolic measurement of each fish was taken c. 20 min after they were placed in the chambers, since a change in measured oxygen concentration in the outflowing water lags behind a corresponding change in activity due to a wash-out effect of the chamber, which in turn is due to a dilution factor (= water inflow rate/ respirometry chamber volume; Frappell, Blevin & Baudinette 1989; Steffensen 1989). This first metabolic measurement was therefore assumed to be a measure of active metabolic rate. The fish were then left overnight so that measurements of SMR could commence 20 h later; by this time they had settled and evacuated their guts (Higgins & Talbot 1985) and any oxygen debt due to differences in activity prior to placing in the chambers would have been paid off. Pilot experiments on juvenile salmon indicated a stable rate of oxygen consumption after this period of acclimation (Cutts 1997; McCarthy 2000). Moreover, the fish were kept in semi-darkness to minimize activity, and the low flow rates (average = 1 6 l h 1 ) through the chambers precluded any active swimming against a current. Measurements of SMR were repeated to give three readings for each fish (with a minimum interval of 30 min between measurements to allow complete flushing of the chamber; see above), and a fourth reading was taken if the initial three values were not in close agreement (i.e. the values being within 10% of the mean value). The entire procedure was identical for each fish, allowing a comparable measure of standard metabolic rate for individuals. After readings of metabolic rate were completed, each fish was measured (fork length, mm) and weighed (g). To calculate whether a fish had relatively high standard metabolic rate, the regression line of absolute oxygen consumption (ml O 2 h 1 ) vs mass (g) plotted on double logarithmic axes was used to calculate the standard metabolic rates that would be expected, given the fish s mass. This was then compared with its observed metabolic rate. A double logarithmic transformation of the data is appropriate for the size range of fish in this study (Yamamoto 1991; see size range below). Furthermore, absolute rather than massspecific values were used, since mass-specific values usually decrease with increasing body size, i.e. larger fish respire less on a per gram basis than smaller fish. The difference between a fish s observed and expected standard metabolic rate was termed the residual SMR (measured in ml O 2 h 1 ). A positive value indicated that a fish had a higher than expected oxygen consumption rate for its size while a negative value indicated a relatively low consumption rate. Factorial metabolic scope was calculated as the ratio of active to standard metabolic rate (AMR/SMR). Both standard and active metabolic rates (and hence metabolic scope) were estimated for 43 juvenile salmon across a mass range of g (mean mass = 3 86 ± 0 21 (= SE) g) kept at an ambient temperature of 9 C. However, in order to obtain highly significant and robust regression equations (P < ) to describe the relationship between standard and active metabolic rate (ml O 2 h 1 ) and fresh body mass (W, g), additional fish (from the same stock and size range and treated identically) were measured for active (14 additional fish) and standard metabolic rates (20 additional fish). Results Regression equations describing the relationship between standard and active metabolic rate (ml O 2 h 1 ) and fresh body mass (W, g) of juvenile salmon were: log e SMR = 0 85 log e W 1 91, eqn 2 (r 2 = 0 575, n = 63, P < ), and log e AMR = 0 83 log e W 1 30, eqn 3 (r 2 = 0 643, n = 57, P < ).

4 76 C. J. Cutts et al. Fig. 1. The relationships between mass (g) and standard (open circles; n = 63) and active (closed circles; n = 57) metabolic rates of juvenile Atlantic Salmon. Both axes are on a natural logarithmic scale. See text for statistical analysis. Fig. 2. The relationship between residual standard metabolic rate (ml O 2 h 1 ) and factorial metabolic scope (active metabolic rate/standard metabolic rate) for juvenile Atlantic Salmon (n = 43). See text for statistical analysis. The standard errors of the mass exponents for equations 2 and 3 were and 0 271, respectively. Analysis of covariance indicated that the slopes of the two lines were not significantly different from each other (F 1,118 = 0 22, P = 0 638). However, there was a significant difference in the elevations of the two lines (F 1,118 = , P < , Fig. 1), active metabolic rate being (not surprisingly) significantly greater than standard metabolic rate. Furthermore (using only fish for which both AMR and SMR were measured), the standard deviation of residual AMR was less than the standard deviation of residual SMR (0 258 and 0 298, respectively [n = 43]), suggesting tighter constraints on variation in AMR than on SMR. Plotting the factorial metabolic scope of individual fish against their residual standard metabolic rates showed a significant negative relationship (r 2 = 0 359, n = 43, P < , Fig. 2). This relationship was independent of body size, since factorial metabolic scope did not vary significantly with fish mass (r 2 = 0 024, n = 43, P = 0 950). Therefore fish with relatively high rates of standard metabolism for their size had low metabolic scopes, i.e. they had a smaller range between their lowest and highest measured rates of metabolism. Discussion Interindividual variation in metabolic rate has previously been shown to influence pairwise relative dominance in juvenile salmon (Metcalfe et al. 1995; Cutts et al. 1999a). Fish with high residual standard metabolic rates tended to be more dominant than those with low residual rates. This variation was unlikely to have been a consequence of agonistic encounters, since dominant juvenile salmon tend also to have larger otoliths (an indicator of higher metabolic rate in salmonids; Mosegaard et al. 1988; Wright 1991) at first feeding (Metcalfe, Wright & Thorpe 1992), several days before the initiation of aggressive behaviour (Dill 1977). Furthermore, individual differences in standard metabolic rate remain consistent over months in juvenile salmonids (McCarthy 2000; Cutts et al. 2001). Standard and active metabolic rates for juvenile salmon showed a similar scaling with body mass (regression exponents: SMR = 0 85, AMR = 0 83), and the regression lines did not differ significantly in slope. There was also no relationship between mass and factorial metabolic scope. This implies that factorial metabolic scope did not increase with body size over the size range of fish in this study ( g), and was in fact independent of mass. Metabolic scope has previously been reported to increase with fish mass in Charr (Salvelinus fontinalis; Beamish 1978), Northern Pike (Esox lucius; Armstrong et al. 1992) and Zebrafish (Brachydario rerio; Lucas & Priede 1992). This study did not concur with their findings. However, the mean factorial metabolic scope of 1 93 presented here is in close agreement with the metabolic scope expected for salmon of this size at the same temperature (Schmidt-Nielsen 1984). Despite evidence from the previously mentioned studies that metabolic scope increases with fish mass, there have also been studies stating that no relationship exists between metabolic scope and mass: Ivlev (1960) reported no difference between the mass exponents of standard and active metabolic rate in juvenile salmon, and Wieser & Forstner (1986) also found no relationship between mass and metabolic scope in juveniles of three species of cyprinid. This may also be due to the different mass ranges used in the studies, since Wieser (1985) has stressed the importance of determining metabolic rate over a wide range of sizes to obtain accurate information on the relationship between metabolic rate and body mass. Conversely, data presenting a single mass exponent for both standard and active metabolism across a wide size range (i.e. from juvenile to adult) must also be treated cautiously, since the mode of activity will often vary with developmental stage. For example, activity is typically of short duration in juvenile fish (e.g. bursts of activity followed by rest) and of longer duration in adults (e.g. sustained swimming) (Post & Lee 1996). Furthermore, variation in AMR was less than that of SMR. This may suggest constraints on the maximum scope for activity: AMR is constrained by the maximum rate that oxygen can be

5 77 Metabolic scope in juvenile salmon transported to respiring tissues (Kaufman 1990), and in fast-growing juvenile fish (as in this study) there will be an additional constraint imposed by the oxygen requirements of growth (Post & Lee 1996). Conversely, the costs of maintenance (measured as SMR) are under no such pressure. On a mass-independent basis, factorial metabolic scope in the present study was negatively correlated with residual standard metabolic rate. This suggests that if the basal, standard metabolic rate is relatively high, there is less scope for activity than if the standard level was lower. This may compromise how individuals allocate available energy. This has implications for Metcalfe et al. s (1995) study on relative standard metabolic rate and dominance, which also used residuals to express interindividual variation in standard metabolic rate, and assumed higher residual values would correspond to a larger metabolic scope. In fact the opposite seems to be the case, since dominant fish appear to have a relatively high cost of maintenance (Priede 1985). Instead of acquiring dominance through a larger metabolic scope and hence capacity for aggressive behaviours, they may instead be aggressive (thus acquiring dominance) in order to gain access to the food that they need to sustain their higher energetic expenditure. Given that a high SMR must be met by enhanced utilization of food and resources, it is unclear what advantage high SMR confers. However, a high SMR causes faster yolk absorption and earlier firstfeeding in juvenile salmon (Metcalfe et al. 1995; Cutts et al. 1999a), in turn leading to earlier feeding territory establishment. This prior residence effect can provide a pronounced advantage in subsequent feeding and growth (Cutts et al. 1999b). Furthermore, since fish with a high SMR and low metabolic scope tend to be more aggressive, they may have a greater food intake overall, with subsequent higher growth. However, it is known that highly aggressive fish can compromise their feeding and growth by spending excessive energy on territorial defence (Elliott 1990; Cutts et al. 2001). While they can reduce their metabolic rate at times of extreme food shortage (O Connor et al. 2000), it may be the case that the metabolic costs of growth are higher in these fish, so that their relatively high SMR can be seen as a cost rather than an advantage. Acknowledgements We thank Vivien Cameron for fish husbandry, BOCM Pauls for supplying fish food, and A. Clarke and J. R. Post for helpful comments on an earlier draft of the manuscript. This study was carried out whilst CJC was in receipt of a NERC studentship, ref. no. GT4/92/ ALS/168. References Armstrong, J.D., Priede, I.G. & Lucas, M.C. 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