Mature, wild sockeye salmon (Oncorhynchus nerka) demonstrated their remarkable stamina and recovery abilities by performing three consecutive critical swimming speed tests with only a 45 min interval for recovery between subsequent tests. Although the repeated swimming challenges were performed without a full recovery, normoxic fish swam just as well on the second swim, and the majority of fish swam only marginally more poorly on the third swim. In addition, metabolic loading in these fish, as measured by the rate of oxygen consumption, ventilation rate and plasma lactate levels during recovery, did not appear to be cumulative with successive swims. Fish, however, did not recover as well after a similar level of initial swimming performance under moderately hypoxic conditions (water mmHg; 1 mmHg=0.1333 kPa). Four out of the five fish did not swim again and their high plasma lactate levels indicated a greater anaerobic effort.

In another group of fish, metabolic loading (elevated control rates of oxygen consumption) was induced with an overnight sublethal exposure to pentachlorophenol, but these fish swam as well as normoxic fish on the first swim, and five of the six fish swam for a third time at a marginally lower critical swimming speed. In contrast to expectations, pentachlorophenol pretreatment and moderate hypoxia were not additive in their effects. Instead, the effects resembled those of pentachlorophenol pretreatment alone. The results are discussed in terms of what aspects of fatigue might impair the repeat swimming performance of sockeye salmon.

The ability of fish to exercise, recover and swim again without hindrance has important ecological ramifications. Even though fish apparently spend most of their time swimming at much slower velocities (Preide and Young, 1977; Tytler, 1978), critical swimming speed (Ucrit; Brett, 1964) is a popular measure of swimming performance because it conveys important information regarding a fish’s ability successfully to forage, to escape predation, to maintain position in a current (Beamish, 1978) and to migrate upstream. For example, the Ucrit of sockeye salmon (Oncorhynchus nerka) has a temperature optimum (Brett, 1971) that corresponds with the ambient water temperature in the Fraser River, British Columbia, when they migrate through the Hell’s Gate rapids (Farrell, 1997). When the river temperature is a few degrees above this optimum, mature sockeye salmon often fail to navigate the rapids and do not reach their spawning grounds. There are, however, many rapids in the Fraser Canyon and since repeat swimming performance, perhaps to exhaustion, is inevitable, a long recovery period could easily be a selective disadvantage.

Information on the recovery period needed for unhindered repeat Ucrit performance is limited. Studies with single and repetitive bouts of exhaustive swimming suggest that recovery may take between 40 min and several hours (e.g. Black, 1955; Brett, 1964, 1965; Stevens and Black, 1966; Turner et al. 1983; Milligan and Wood, 1986; Scarabello et al. 1991, 1992; Arthur et al. 1992; Pagnotta et al. 1994; for a review, see Wood, 1991). For example, following a single 5 min exhaustive burst swim in rainbow trout (Oncorhynchus mykiss), the oxygen debt was repaid in 2–3 h (Scarabello et al. 1992). Similarly, following Ucrit swimming, oxygen debt was repaid in 3.2 h in sockeye salmon and over a somewhat longer period in coho salmon (Oncorhynchus kisutch) (Brett, 1964). Furthermore, because burst exercising at intervals up to 1 h resulted in almost additive metabolic effects and culminated in a refusal to swim, Stevens and Black (1966) concluded that rainbow trout do not tolerate frequent periods of exercise of short duration. However, because all accumulated lactate need not be oxidized before the fish can swim again (Hochachka, 1961), full metabolic recovery is not necessary for repeat swimming performance. In fact, a few studies indicate that salmonids can swim to the same Ucrit after less than 2 h of recovery. For example, chinook salmon (Oncorhynchus tshawytscha) at 10 °C performed equally well when two Ucrit tests were separated by 60 min (Randall et al. 1987), as did wild juvenile coho salmon using a 2 h recovery period (Brauner et al. 1994). Similarly, the recovery period was 70 min for hatchery-reared rainbow trout swimming in fresh water at 8–9 °C and only 40 min for preliminary experiments with mature, wild sockeye salmon swimming in fresh water at 19 °C (Jain et al. 1998). Peake et al. (1997) suggested that the recovery times and recovery speeds prior to Ucrit testing and following handling stress in juvenile rainbow trout may have been too conservative.

The present study characterises for the first time the ability of mature, wild sockeye salmon to perform three consecutive swim challenges separated by short (45 min) recovery periods in a situation that mimicked certain aspects of their spawning migration (i.e. the transition to fresh water and a high water temperature). We also examined the degree to which metabolic loading affected recovery. To do this, fish were stressed with moderately hypoxic water during the first swim and/or with a sublethal exposure (12–14 h) to pentachlorophenol prior to the first swim.

Fish capture and maintenance

On 9 and 16 July 1996, mature sockeye salmon (aged 4+ to 5+ years) were captured in Alberni Inlet on the west coast of Vancouver Island (British Columbia, Canada) by a commercial seiner and placed into the ship’s seawater hold. At the Port Alberni wharf, these fish were transferred to an insulated fibreglass tank for transport by truck to the West Vancouver Laboratory (WVL), British Columbia (Department of Fisheries and Oceans, Canada). To reduce stress, individual fish were handled with a low-abrasion dipnet, and the transport tank contained oxygenated, chilled iso-osmotic water (2 parts sea water to 1 part fresh water; 6.4–9.8 °C) with 0.25 mg l−1 of the anaesthetic metomidate hydrochloride (Syndel Laboratories, Vancouver, British Columbia, Canada) and 500 g of the ammonia-binding clay Ammorex (Argent Chemical Laboratories, Redmond, WA, USA). At the WVL, fish were kept at a density of 2 kg m−3 or less in outdoor 3500 l round fibreglass tanks continuously supplied with air-equilibrated sea water (10.0–12.9 °C). As a therapeutic treatment for suspected seawater vibriosis as well as a prophylactic treatment against bacterial disease and fin rot, all fish were exposed for 1 h to Chloramine-T (N-sodium-N-chloro-p-toluenesulphonamide; 8.5 mg l−1) in an aerated static bath. A second treatment was administered 24 h later. Fish were held for at least a further 3 weeks before experimentation at Simon Fraser University (SFU) and were not fed after capture.

Groups of three or four fish were transported to SFU in a 1 m3 insulated transport tank containing aerated iso-osmotic water. At SFU, fish were placed into a 1600 l outdoor annular fibreglass raceway (length 343 cm, depth 41 cm, width 46 cm) filled with iso-osmotic water that was gradually replaced with dechlorinated Vancouver municipal fresh water at a flow rate of 5 l min−1. The salinity in the annular raceway was reduced to less than 3 ‰ over approximately 10–12 h. Ambient water temperature in the raceway ranged from 15.6 to 18.6 °C over the study period.

Cannulation and transfer to the swim-tunnel

Soon (24–36 h) after the salmon had been transported to SFU, they were briefly anaesthetized in MS-222 (0.2 g l−1) buffered with NaHCO3. Fish mass, fork length (BL), maximum width and maximum depth were measured and the fish were placed supine on a surgical table to allow for dorsal aortic cannulation (PE 50; Smith and Bell, 1967) while under anaesthesia (0.1 g l−1 buffered MS-222). Following the 3–5 min cannulation procedure, fish were either placed directly into a 130 l Brett-type swim-tunnel respirometer (see Gehrke et al. 1988), supplied with dechlorinated water at a rate of 3 l min−1, or returned to the outdoor tank for up to 3 days before experimentation. When transferring fish from the outdoor tank to the respirometer, they were briefly and lightly anaesthetized with buffered MS-222.

Experimental protocols

Fish recovered for 30 min in the swim-tunnel before a brief swim to habituate them to increases in current velocity (Jain et al. 1997). In this initial swim, current velocity was gradually increased to 1 BL s−1 over 10–15 min and was then maintained at 0.4 BL s−1 overnight. A water of 150 mmHg (20 kPa) was achieved in the respirometer by passing the incoming water through a gas-exchange column receiving a controlled mixture of air and oxygen. Water was monitored overnight and during subsequent Ucrit tests by continuously withdrawing water from the respirometer using a peristaltic pump (Masterflex, Chicago, IL, USA) and passing it through a thermostatted electrode (Radiometer, model E5046-0, Copenhagen, Denmark).

After an overnight habituation for 12–14 h at 0.4 BL s−1, the water temperature was raised from ambient to 19–20 °C over a 1 h period using a heat-exchange column of local construction. Three successive critical swimming speed tests (Ucrit1, Ucrit2 and Ucrit3) were then carried out for each fish at this temperature. These tests were separated by 45 min recovery periods during which water velocity was maintained at 0.4 BL s−1. In our Ucrit protocol, current velocity was gradually increased to 40 cm s−1 (approximately 0.6 BL s−1) over 15 min. Thereafter, current velocity was increased by 12.5 cm s−1 (approximately 0.25 BL s−1) every 15 min until the fish fatigued. This protocol produces Ucrit values similar to those obtained using more standard protocols in which current velocity increments are constant throughout (Jain et al. 1997). Exhaustion was established by the inability of the fish to swim away from the electrified (5 V) grid at the rear of the swim chamber after three short shocks. Ucrit was calculated as described by Brett (1964). When necessary, Ucrit values were corrected for the solid blocking effects (Bell and Terhune, 1970). At the end of the experiment, fish were humanely killed by an overdose of the fish anaesthetic and cervical dislocation. The ventricle was removed, blotted with a paper towel and weighed. Relative ventricular mass was calculated from the ventricular mass and fish mass.

Experimental groups

Twenty-one fish were randomly assigned to one of four experimental groups, and each group had similar morphometrics, haematocrit and leucocrit (Table 1). Normoxic fish (N=5) performed the three Ucrit tests, as described above, under normoxic conditions. Hypoxic fish (N=5) were made moderately hypoxic (a water of 100–106 mmHg=13.3–18.8 kPa) for the Ucrit1 test by reducing the rate of oxygenation in the gas-exchange column once the water temperature in the swim-tunnel had. reached 19–20 °C. These fish also had their post-exercise measured under hypoxic conditions. Thereafter, water was increased to 150 mmHg within 5 min and maintained at a normoxic level for the remainder of the recovery period and during subsequent swim tests. The protocol used for normoxic fish pretreated with pentachlorophenol (PCP) (N=6) was identical to that used for normoxic fish except that the fish were pre-exposed overnight to a sublethal concentration of PCP (13.7±1.0 μg l−1; mean ± S.E.M.) in the water (Webb and Brett, 1973; NRCC, 1982). The median lethal concentration, killing 50 % of juvenile sockeye salmon in 96 h, is 63 μg l−1 (Webb and Brett, 1973). Also, the half-time for PCP disappearance from the blood of rainbow trout after an intraarterial injection is about 5 h (Chris Kennedy, personal communication). Toxicant was flushed from the respirometer for at least 1 h prior to increasing the water temperature in the swim-tunnel. The protocol used with hypoxic fish pretreated with PCP (N=5) was identical to that for hypoxic fish except that the fish were also pre-exposed to PCP (13.7±1.3 μg l−1; mean ± S.E.M.) as described above.

Table 1.

Morphometric and haematological variables in the different test groups of mature sockeye salmon Oncorhynchus nerka

Morphometric and haematological variables in the different test groups of mature sockeye salmon Oncorhynchus nerka
Morphometric and haematological variables in the different test groups of mature sockeye salmon Oncorhynchus nerka

Toxicant preparation and measurement

A stock solution of sodium pentachlorophenate (23 mg l−1) was prepared by dissolving 2.0 g of NaOH and 46.6 mg of PCP in 2 l of double-distilled water (Webb and Brett, 1973). This solution was diluted 1:19 with dechlorinated water just prior to use and was delivered to the swim-tunnel using a pre-calibrated peristaltic pump at a rate of 10 ml min−1 to bring the PCP water concentration in the swim-tunnel to a nominal 20 μg l−1 within 15 min. Pumping rate was then adjusted to 2 ml min−1 for 12–14 h to maintain the PCP concentration. The actual PCP concentration reported above was based on 1 l water samples taken at the end of each exposure period. These samples were stored in the dark at 4 °C until they were analyzed at the Analytical Chemistry Laboratory (Organics), Pacific Environmental Science Centre, Environment Canada, North Vancouver, British Columbia.

and other physiological measurements

was measured on. seven occasions during the experiment. Control (rest) was measured prior to Ucrit1 while the fish was swimming at a current velocity of 0.4 BL s−1 at 19–20 °C. Post-exercise was measured during the 10 min period immediately following each of the three Ucrit tests during which the current velocity was 0.4 BL s−1. Recovery was measured during the last 10 min of the 45 m. in recovery period following each of the three swim tests. was calculated from the measured decrease in water over an 8–10 min period with the respirometer closed. Duplicate water samples were taken from the swim-tunnel at the beginning and end of the measurement period and injected into a second Radiometer electrode (model E5046-0, Copenhagen, Denmark) to measure the decrease in water . At the end of each measurement, the water was rapidly restored (over a 5 min period) by flushing the swim-tunnel with oxygenated water.

Ventilation rate (min−1) was recorded towards the end of the measurement by counting opercular movements for 45 s. Blood samples (1.0 ml) were withdrawn from the dorsal aorta to measure haematocrit, leucocrit, arterial blood and plasma lactate concentration. Haematocrit and leucocrit were determined on 20 μl blood samples following centrifugation at 10 000 g for 2 min. was measured using a thermostatted Radiometer electrode (model E5046-0, Copenhagen, Denmark) connected to a Gould chart recorder (model 2200, Cleveland, OH, USA). Plasma, obtained by centrifugation of whole blood at 10 000 g for 1 min, was quickly frozen in liquid nitrogen and stored at −80 °C. Plasma lactate concentrations were determined on duplicate 10 μl plasma samples using colorimetry (Sigma Diagnostics, St Louis, MO, USA). Following centrifugation, the remaining red blood cells were resuspended in 0.8 ml of saline and returned to the fish through the dorsal aortic cannula.

Data analysis

The recovery ratio for Ucrit was calculated by dividing either Ucrit2 or Ucrit3 by Ucrit1. Mean values are presented with the standard error of the mean (S.E.M.). Statistical comparisons were performed using a software package (SYSTAT Inc.). A one-way repeated-measures analysis of variance (ANOVA) was used for comparisons involving repeated sampling, and a one-way ANOVA was used for comparisons among test groups. Multiple comparisons were made using Fisher’s least-squares difference (LSD). Linear regression analysis was used for the correlations. P<0.05 was used to establish statistical significance.

Normoxic fish

After overnight habituation to the swim-tunnel, control was 2.10±0.19 ml O2 kg−1 min−1 and ventilation rate was 69.8±6.9 min−1 (Figs 1, 2). Plasma lactate concentration was 1.0±0.5 mmol l−1 and was 110±6 mmHg (Figs 3, 4). Ucrit1 for normoxic fish was 1.44±0.09 BL s−1 (Fig. 5).

Fig. 1.

The rate of oxygen uptake

(V·O2)
of mature sock-eye salmon (Oncorhynchus nerka) prior to, during and after, three consecutive swimming challenges separated by 45 min recovery periods. The results for the four treatment groups are presented separately. Rest, presented separately. Rest, exercise and recovery refer to the value prior to the first swim, the value immediately post-exercise and the value at the end of the 45 min recovery period, respectively. Numbers (1, 2 and 3) denote the first, second and third swims. The numbers located immediately under each column are the numbers of fish tested, and the vertical bars represent S.E.M. An asterisk denotes a significant difference (P<0.05) from the rest value within a test group. Similar letters denote a significant difference (P<0.05) between comparable values among test groups. PCP, pentachlorophenol.

Fig. 1.

The rate of oxygen uptake

(V·O2)
of mature sock-eye salmon (Oncorhynchus nerka) prior to, during and after, three consecutive swimming challenges separated by 45 min recovery periods. The results for the four treatment groups are presented separately. Rest, presented separately. Rest, exercise and recovery refer to the value prior to the first swim, the value immediately post-exercise and the value at the end of the 45 min recovery period, respectively. Numbers (1, 2 and 3) denote the first, second and third swims. The numbers located immediately under each column are the numbers of fish tested, and the vertical bars represent S.E.M. An asterisk denotes a significant difference (P<0.05) from the rest value within a test group. Similar letters denote a significant difference (P<0.05) between comparable values among test groups. PCP, pentachlorophenol.

Fig. 2.

The ventilation rate of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 2.

The ventilation rate of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 3.

The plasma lactate levels of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 3.

The plasma lactate levels of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 4.

The arterial blood partial pressure of oxygen

(PaO2)
(1 mmHg=0.1333 kPa) of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 4.

The arterial blood partial pressure of oxygen

(PaO2)
(1 mmHg=0.1333 kPa) of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 5.

The swimming performance (Ucrit) of mature sockeye salmon (Oncorhynchus nerka) for three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details. Similar letters denote a significant difference (P<0.05) within test groups. BL, fork length.

Fig. 5.

The swimming performance (Ucrit) of mature sockeye salmon (Oncorhynchus nerka) for three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details. Similar letters denote a significant difference (P<0.05) within test groups. BL, fork length.

Following the first swim, post-exercise ventilation rate and plasma lactate concentration were all significantly elevated two- to fourfold (Figs 13). did not change significantly (Fig. 4). At the end of the 45 min recovery period, and ventilation rate had returned to their control values (Figs 1, 2). However, was significantly elevated compared with the control value (Fig. 4), and the plasma lactate level tended to be higher at 4.4±1.3 mmol l−1 (but P>0.05) (Fig. 3). All five fish swam equally well after the 45 min recovery period. Ucrit2 was not significantly different from Ucrit1 (Fig. 5), and the recovery ratio of 0.97±0.02 was not significantly different from unity.

Variables measured during the second post-exercise recovery period showed similar patterns to those observed following the first swim (Figs 15). An exception to this generalization was a significant post-exercise decrease in compared with the value during the first recovery period (Fig. 4). Also, the plasma lactate levels were unchanged compared with the first recovery period, and the high variance, mainly because one fish had an especially high (>8 mmol l−1) lactate value, obscured a statistical difference compared with control values.

Three out of the five normoxic fish swam for a third time. Individual recovery ratios were 0.93, 0.95 and 0.67 for Ucrit3, and the mean value of 0.85±0.09 was significantly different from unity. Interestingly, those fish that swam a third time had post-exercise and recovery plasma lactate levels that were less than 2.0 mmol l−1 during the second recovery period, whereas individuals with higher plasma lactate values did not swim for a third time (Fig. 3).

Normoxic fish pre-treated with PCP

After overnight exposure to PCP, control in clean, normoxic water (3.41±0.29 ml O2 kg−1 min−1) was elevated by 50 % compared with that of normoxic fish (Fig. 1), but plasma lactate level, and ventilation rate were unchanged (Figs 24). Despite this metabolic load, PCP-treated fish swam just as well as normoxic fish. Ucrit1 was 1.28±0.11 BL s−1 (Fig. 5). Moreover, all six PCP-treated fish swam a second time following a 45 min recovery period. Although Ucrit2 (1.19±0.11 BL s−1) was not significantly different from Ucrit1 (Fig. 5), the recovery ratio of 0.93±0.04 for Ucrit2 was significantly different from unity. Thus, the recovery ratio proved to be a more sensitive index of the subtle impairment on repeat swimming performance of PCP treatment.

Many of the variables measured in PCP-treated fish during the first recovery period changed in a manner qualitatively and quantitatively similar to that already described for normoxic fish. However, there were important differences, and these all point to Ucrit1 producing a greater metabolic loading in PCP-treated fish. Notably, ventilation rate, and plasma lactate level remained significantly elevated during the recovery period compared with the control values, unlike values in the normoxic fish (Figs 13). Surprisingly, therefore, a greater proportion of PCP-treated fish (five out of six) swam for a third time compared with normoxic fish, and Ucrit3 was not significantly different from Ucrit1. Nonetheless, the individual recovery ratios for Ucrit3 were 0.98, 0.97, 0.96, 0.88 and 0.80 and the group mean was 0.92±0.03, a value significantly lower than unity. Consequently, the significant metabolic load of sublethal PCP pretreatment had only a marginal negative effect on repeat swimming performance of mature sockeye salmon.

Fish performing the initial swim under moderately hypoxic conditions

Compared with normoxic fish, exposure to moderate hypoxia (water ) prior to the first swim significantly decreased (83±8 mmHg) and increased ventilation rate (103±14 min−1) (Figs 2, 4) without affecting control control plasma lactate level and Ucrit1 (1.19±0.13 BL s−1) (Figs 1, 3, 5). The swimming effort under moderate hypoxia elevated plasma lactate levels both immediately post-exercise (6.24 mmol l−1) and after the 45 min recovery period (10.8 mmol l−1) compared with that of normoxic fish (Fig. 3). Furthermore, repeat swimming ability was very poor. Four out of five fish did not swim again in normoxic water (Fig. 5). Plasma lactate level was followed in two of these fish for the next 45 min and remained significantly elevated (between 7.8 mmol l−1 and 17.8 mmol l−1) despite a normal . One fish in this group did swim three times, and Ucrit2 and Ucrit3 in normoxic water were higher than Ucrit1 in hypoxic water (the recovery ratios were 1.32 and 1.29 for Ucrit2 and Ucrit3, respectively). This fish turned out to be the best individual swimmer of all the 21 fish tested (Fig. 5).

PCP-treated fish performing the initial swim under moderately hypoxic conditions

Because hypoxia severely impaired recovery, and because PCP pretreatment reduced the recovery ratio, the expectation was that these negative effects would be additive. This was not true. In fact, it appeared that PCP pretreatment ameliorated the effect of swimming in moderate hypoxia. Four out of five PCP-treated hypoxic fish swam three times, and plasma lactate levels were no more elevated compared with the post-exercise and recovery values for the normoxic and normoxic PCP-treated fish (Fig. 3). These findings clearly contrast with those for fish exposed to hypoxia alone. However, this level of performance was not maintained for the third swim. Ucrit3 under normoxic conditions (1.21±0.06 BL s−1) was significantly lower than Ucrit2 (1.35±0.06 BL s−1) and was no better than Ucrit1 under hypoxic conditions (1.21±0.04 BL s−1).

Regression analyses

The limited supply of wild, mature sockeye salmon may have diminished the power of certain statistical comparisons among treatment groups. Therefore, data were pooled for regression analysis, the results of which are summarised in Table 2. The significant correlations between control lactate level and and between ventilation rate and were perhaps not surprising for some of the test groups. However, the finding that Ucrit1 was correlated both with plasma lactate level (for all hypoxic fish) and with haematocrit (for normoxic, hypoxic and PCP-treated fish) was important, as was the unexpectedly strong correlation coefficient for the regression between ventilation rate and for all but the hypoxic grouping (Table 2). A number of significant regressions were found by pooling all treatment groups. As might be expected, ventilation rate was positively correlated with at rest (r =0.37), on first recovery (r2=0.37) and on second recovery (r2=0.54). Also, given the high recovery ratios for most fish, the correlations between Ucrit1 and Ucrit2 (r2=0.25) and between Ucrit2 and Ucrit3 (r2=0.49) were not surprising. Likewise, the negative correlation between and ventilation rate at rest (r2=0.50) was expected. Some predictive correlations were also revealed. For example, Ucrit1 was negatively correlated with both ventilation rate at rest and at rest (Fig. 6), suggesting that the effect of metabolic loading on Ucrit was too subtle to be revealed by comparisons of mean values. Similarly, haematocrit at rest was positively correlated with Ucrit1 (Fig. 6), even though mean haematocrit values were unchanged (Fig. 7). A positive relationship between haematocrit and Ucrit has been demonstrated previously by some (Gallaugher et al. 1995) but not all researchers (Jones, 1971).

Table 2.

Summary of the regression analyses for control variables measured in mature sockeye salmon Oncorhynchus nerka

Summary of the regression analyses for control variables measured in mature sockeye salmon Oncorhynchus nerka
Summary of the regression analyses for control variables measured in mature sockeye salmon Oncorhynchus nerka
Fig. 6.

Regression analyses for some variables that were found to be significantly correlated with Ucrit1 in mature sockeye salmon (Oncorhynchus nerka). Data from all four test groups were combined for these analyses. ○ normoxic; ▫, PCP-treated; △ hypoxic PCP-treated; ▽, hypoxic; PCP, pentachlorophenol.

Fig. 6.

Regression analyses for some variables that were found to be significantly correlated with Ucrit1 in mature sockeye salmon (Oncorhynchus nerka). Data from all four test groups were combined for these analyses. ○ normoxic; ▫, PCP-treated; △ hypoxic PCP-treated; ▽, hypoxic; PCP, pentachlorophenol.

Fig. 7.

The haematocrit of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

Fig. 7.

The haematocrit of mature sockeye salmon (Oncorhynchus nerka) before and following three consecutive swimming challenges separated by 45 min recovery periods. See Fig. 1 and the text for other details.

The primary goal of this investigation was to examine the repeat swimming performance of mature, wild sockeye salmon subjected to three consecutive Ucrit tests separated by 45 min recovery periods. The results show rather convincingly that normoxic sockeye salmon can repeat the same Ucrit performance with only a short recovery period and that the metabolic loading associated with PCP pretreatment had no significant effect on repeat Ucrit performance. These findings are consistent with earlier studies using either similar or longer recovery periods and with either a similar (rainbow trout and sockeye salmon, Jain et al. 1998) or a different (chinook salmon, Randall et al. 1987; coho salmon, Brauner et al. 1994) protocol. Collectively, these results show the remarkable ability of healthy salmonids to repeat their swimming performance. A novel finding is that 60 % of the normoxic fish and 80 % of the normoxic PCP-treated fish swam for a third time at 92–93 % of their normal Ucrit.

New information was provided on the recovery of , ventilation rate and plasma lactate level following repeat swimming. Our data clearly show that complete recovery of these metabolic indicators was not necessary for repeat Ucrit performance. Normoxic fish repeated their swimming performance with an elevated plasma lactate level, and PCP-pretreated fish repeated their swimming performance with an elevated plasma lactate level, ventilation rate and Stevens and Black (1966) reported that 5 min bouts of burst swimming every hour ultimately prevented subsequent swimming in salmonids, and Scarabello et al. (1992) reported that as long as a full metabolic correction from a first bout of exercise had occurred, a second bout was better tolerated. Collectively, these studies point to two important concepts: (a) metabolic disturbances associated with swimming to fatigue must reach a threshold level before having a negative impact on repeat Ucrit swimming; and (b) repeat swimming can lead to training effects. These two concepts are now discussed within the context of the present study.

Swimming to Ucrit in salmonids involves aerobic metabolism at lower speed and increasingly more anaerobic metabolism as the fish nears Ucrit (Jones, 1981; Day and Butler, 1996). Plasma lactate level is an indicator of the anaerobic swimming effort (Black, 1955) and, as the following discussion shows, could be useful to indicate a level of fatigue that inhibits repeat swimming. Although swimming to Ucrit1 elevated plasma lactate level, the second and third swims to at least 90 % of Ucrit1 produced no further accumulation of plasma lactate in three of the groups tested. A similar finding has been reported for a second swim in sockeye salmon (Jain et al. 1998). These data suggest that the anaerobic contribution to repeat Ucrit swimming did not increase, otherwise plasma lactate level would have been higher for subsequent swims. The present data cannot establish why lactate did not accumulate in the plasma, but possibilities include a greater reliance on aerobic swimming and using lactate as a fuel during the lower speeds of repeat swimming. Instead, an important observation is that repeat swimmers generally maintained plasma lactate level at less than 5 mmol l−1, whereas plasma lactate levels were twice as high when sockeye salmon swam in moderately hypoxic water. This greater anaerobic swimming effort for Ucrit1 under hypoxic conditions resulted in an extremely poor repeat swimming ability. Since most of this group refused to swim again even at low swimming speeds, it is likely that aerobic muscle activity was impaired. The refusal of sockeye salmon to swim was characterised by plasma lactate levels above 10 mmol l−1 and, similarly, rainbow trout refused further repetitive burst swimming when plasma lactate level had reached 13 mmol l−1 (muscle lactate level was 52 mmol l−1) (Stevens and Black, 1966) Thus, given that these two studies used different types of swimming tests, it appears that a plasma lactate level above 10 mmol l−1 may be indicative of a level of fatigue that prohibits repeat swimming within an hour.

The proximate cause of fatigue in fish awaits further study. Indeed, the degree to which metabolic and psychogenic factors lead to fatigue still needs some resolution. However, because our fish swam after a 45 min recovery, and because muscle glycogen level, pH and lactate level recover at a slower rate following exhaustive burst exercise (Milligan and Wood, 1986; Scarabello et al. 1992), these metabolic parameters are poor candidates. In contrast, muscle creatine phosphate and ATP levels may be more important because they can recover from a 70 % reduction within 1 h post-fatigue. Elevated ammonia levels are also associated with reduced Ucrit performance in brown trout (Salmo trutta) (Beaumont et al. 1995; Day and Butler, 1996), but we know little of the recovery rate for ammonia other than that the post-exercise increase in ammonia excretion lasts for 2–4 h (Scarabello et al. 1992).

Interestingly, our fish either refused to swim for a third time or swam approximately 10–20 % slower for Ucrit3. Thus, there may be two metabolic thresholds for repeat swimming rather than one. A higher threshold, indicated by plasma lactate levels greater than 10 mmol l−1, could signal the fatigue that prevents repeat swimming. A lower metabolic threshold might inhibit anaerobic swimming, explaining why Ucrit decreased by approximately 10–20 % and why plasma lactate did not accumulate beyond 3–4 mmol l−1 with repeat Ucrit swimming. Inhibition of white muscle recruitment during swimming is not a novel suggestion since it has been shown that acidic water reduces the Ucrit of brown trout in this manner (Day and Butler, 1996).

Training effects are reported for both short-term (Farlinger and Beamish, 1977) and long-term (e.g. Pearson et al. 1990; Farrell et al. 1990; Thorarensen et al. 1993) studies and even include, in the long term, an improved ability to defend against the osmotic imbalance (Gallaugher, 1994) associated with swimming (Wood, 1991). In the short term, Scarabello et al. (1992) suggested that the faster rates of recovery of lactate, creatine phosphate and respiratory gases for a second exhaustive burst exercise bout, and possibly the fact that the fish were less psychologically disturbed through learning, were training effects. Other short-term training effects are clearly possible. One possibility is that metabolic recovery and repayment of the O2 debt could occur at low swimming speeds during subsequent exercise bouts. In this case, for a given swimming speed would be higher for a repeat swim compared with that for an initial swim, a possibility that could be tested experimentally. A second possibility is that the locomotory muscles could operate more efficiently for repeat swimming (i.e. a reduction in the skeletal muscle O2 requirement for the same work output) and thus compensate for a metabolic load accumulated with Ucrit1. Unfortunately, this possibility will be difficult to distinguish experimentally from a third possibility, namely that the metabolic requirements of non-locomotory tissues can be either reduced or temporarily suspended during swimming and recovery (‘multitasking’) so as to divert blood flow and O2 to locomotory muscles. This possibility has good experimental support. Chinook salmon decrease their blood flow to the gut as swimming speed and increase, and trained fish are better able to maintain gut blood flow during swimming than untrained fish (Thorarensen et al. 1993). Clearly, salmonids must, and do, make decisions about how to multitask their O2 requirements with exercise. How they do so, what the limits are and how training influences these demands will require much more research.

Implicit in the above discussion is the idea that maximum is attained at Ucrit. If this were not the case, then a higher at Ucrit2 compared with Ucrit1 might preclude the need for full metabolic recovery. Many studies have suggested that active metabolic r.ate in salmonids provides a reliable measure of maximum (e.g. Brett, 1971; Beamish, 1978; Thorarensen et al. 1993; Gallaugher et al. 1995), but perhaps the best experimental evidence for this comes from the finding that post-prandial . swimming in salmonids lowered Ucrit without affecting (Thorarensen, 1994; Alsop and Wood, 1997). Conversely, therefore, post-prandial metabolism can compromise the ability of locomotory muscle to ‘steal’ O2 from other tissues but, because does not increase beyond the level normally encountered at Ucrit, swimming can also compromise the efficiency and speed of digestion (see Jobling, 1981). was not measured at Ucrit in the present study, but had for Ucrit2 been elevated, it is likely that the second post-exercise would also have been elevated; this was not the case. Furthermore, Jain et al. (1998) observed a similar at Ucrit2 compared with that at Ucrit1 in an earlier study with mature sockeye salmon. However, in non-salmonid species such as the Atlantic cod (Gadus morhua) .and large-mouth bass (.Micropterus salmoides), post-prandial and post-exercise may be better indicators of their metabolic scope (Beamish, 1974; Jobling, 1981; Soofiani and Priede, 1985; Reidy et al. 199.5). There is also evidence that, under certain circumstances, and Ucrit may not remain tightly coupled in salmonids (i.e. that at Ucrit is not equal to ). Although parallel effects of haematocrit on maximum and Ucrit are observed in anaemic and normocythaemic rainbow trout, this was not the case when the fish were made polycythaemic (Gallaugher et al. 1995).: Ucrit increased slightly with haematocrit, whereas maximum reached a plateau.

PCP, a mitochondrial uncoupling agent (NRCC, 1982), was expected to create a metabolic load and limit Ucrit. Previously, Beamish (1978) has discussed how environmental challenges can load and limit metabolism. In fact, elevated temperature, hypoxia, disease and toxicant exposure have all been shown to decrease Ucrit (Brett and Glass, 1973; Waiwood and Beamish, 1978; Thomas and Rice, 1987; Butler and Day, 1993; Nikl and Farrell, 1993; Beaumont et al. 1995; for a review, see Fry, 1971). Therefore, we have no explanation for why although control increased by 50 % during PCP pretreatment (a) Ucrit1 was unchanged, (b) a higher proportion of normoxic PCP-treated fish performed repeat swimming compared with normoxic fish, and (c) the negative impact of an initial hypoxic swim was ameliorated. Although PCP can be removed from fish placed in clean water, the half-time for clearing PCP from the plasma of rainbow trout suggests that PCP effects would be present for at least the first two swim challenges. Previously, Holmberg and Saunders (1979) found that a 4 day treatment with 0.1 mg l−1 PCP elevated by approximately twofold in American eels (Anguilla rostrata) and elevated the O2 cost of slow-speed (35 cm s−1) swimming (Ucrit was not tested). In juvenile sockeye salmon, sublethal PCP exposure did not reduce Ucrit, but reduced growth rate and food conversion efficiency (Webb and Brett, 1973), presumably as a result of the elevated resting metabolic rate.

As with previous studies, the moderate hypoxia experiments illustrated that repeat swimming performance is a valuable and sensitive measure of physiological impairment. Diseased mature sockeye salmon had a recovery ratio of 0.6 instead of 1.0, and pretreatment with a resin acid significantly reduced the recovery ratio to 0.92 and elevated control (Jain et al. 1998). Also, we have estimated recovery ratios from the data of Brauner et al. (1994) for juvenile coho salmon following acute transfer to sea water. The recovery ratios were 0.96 and 0.94, respectively, for both wild and hatchery-reared fish tested in fresh water and were reduced to 0.86 and 0.82, respectively, following acute transfer to sea water. Thus, it appears that the metabolic loading associated with transfer to salt water was sufficiently large to impair recovery performance.

In conclusion, sockeye salmon performed three consecutive Ucrit tests separated by short recovery intervals. A full metabolic recovery was not necessary for repeat Ucrit swimming performance. Although plasma lactate levels appeared to be a useful index of repeat swimming capabilities, more studies are need to explain more fully the remarkable repeat swimming capability of sockeye salmon.

The authors would like to thank Jim Mitchell for providing for our use of the Department of Fisheries and Oceans test fishery purse seine vessel Viking Spirit, and acknowledge the captain and crew of this vessel for their skilful cooperation. At the Department of Fisheries West Vancouver Laboratory, we thank Jill Korstrom, Susanne Spohn and Ron Fink for fish care during transfer and holding. At Simon Fraser University, we thank Keith Tierney for lactate analysis and Stephen Peake for statistical analysis. Also, we are grateful to R. Strub of Environment Canada’s Pacific Environmental Science Centre for analysis of PCP samples. This study was funded by the Federal Government’s Toxic Chemicals Green Plan and a Natural Science and Engineering Research Council of Canada grant to A.P.F.

Alsop
,
D. H.
and
Wood
,
C. M.
(
1997
).
The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss)
.
J. exp. Biol
.
200
,
2337
2346
.
Arthur
,
P. G.
,
West
,
T. G.
,
Brill
,
R. W.
,
Schulte
,
P. M.
and
Hochachka
,
P. W.
(
1992
).
Recovery metabolism of skipjack tuna (Katsuwonus pelamis) white muscle: rapid and parallel changes in lactate and phosphocreatine after exercise
.
Can. J. Zool
.
70
,
1230
1239
.
Beamish
,
F. W. H.
(
1974
).
Apparent specific dynamic action of largemouth bass, Micropterus salmoides
.
J. Fish. Res. Bd Can
.
31
,
1763
1769
.
Beamish
,
F. W. H.
(
1978
).
Swimming capacity
.
In Fish Physiology
, vol.
7
(ed.
W. S.
Hoar
and
D. J.
Randall
), pp.
101
187
.
New York
:
Academic Press
.
Beaumont
,
M. W.
,
Butler
,
P. J.
and
Taylor
,
E. W.
(
1995
).
Exposure of brown trout, Salmo trutta, to sub-lethal copper concentrations in soft acidic water and its effect upon sustained swimming performance
.
Aquat. Toxicol
.
33
,
45
63
.
Bell
,
W. H.
and
Terhune
,
L. D. B.
(
1970
).
Water tunnel design for fisheries research
.
Fish. Res. Bd Can. Tech. Report
195
,
1
169
.
Black
,
E. C.
(
1955
).
Blood levels of hemoglobin and lactic acid in some freshwater fishes following exercise
.
J. Fish. Res. Bd Can
.
12
,
917
929
.
Brauner
,
C. J.
,
Iwama
,
G. K.
and
Randall
,
D. J.
(
1994
).
The effect of short-duration seawater exposure on the swimming performance of wild and hatchery-reared juvenile coho salmon (Oncorhynchus kisutch) during smoltification
.
Can. J. Fish. aquat. Sci
.
51
,
2188
2194
.
Brett
,
J. R.
(
1964
).
The respiratory metabolism and swimming performance of young sockeye salmon
.
J. Fish. Res. Bd Can
.
21
,
1183
1226
.
Brett
,
J. R.
(
1965
).
The relation of size to rate of oxygen consumption and sustained swimming performance of sockeye salmon (Oncorhynchus nerka)
.
J. Fish. Res. Bd Can
.
22
,
1491
1501
.
Brett
,
J. R.
(
1971
).
Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka)
.
Am. Zool
.
11
,
99
113
.
Brett
,
J. R.
and
Glass
,
N. R.
(
1973
).
Metabolic rates and critical swimming speeds of sockeye salmon, Oncorhynchus nerka, in relation to size and temperature
.
J. Fish. Res. Bd Can
.
30
,
379
387
.
Butler
,
P. J.
and
Day
,
N.
(
1993
).
The relationship between intracellular pH and swimming performance of brown trout exposed to neutral and sublethal pH
.
J. exp. Biol
.
176
,
271
284
.
Day
,
N.
and
Butler
,
P. J.
(
1996
).
Environmental acidity and white muscle recruitment during swimming in the brown trout (Salmo trutta)
.
J. exp. Biol
.
199
,
1947
1959
.
Farlinger
,
S.
and
Beamish
,
F. W. H.
(
1977
).
Effects of time and velocity increments on the critical swimming speed of largemouth bass
.
Trans. Am. Fish. Soc
.
106
,
436
439
.
Farrell
,
A. P.
(
1997
).
Effects of temperature on cardiovascular performance
.
In Global Warming Implications for Freshwater and Marine Fish
(ed.
C. M.
Wood
and
D. G.
Mcdonald
), pp.
135
158
.
Cambridge
:
Cambridge University Press
.
Farrell
,
A. P.
,
Johansen
,
J. F.
,
Steffensen
,
C. D.
,
Moyes
,
T. G.
and
Suarez
,
R. K.
(
1990
).
Effects of exercise-training and coronary ablation on swimming performance, heart size and cardiac enzymes in rainbow trout, Oncorhynchus mykiss
.
Can. J. Zool
.
68
,
1174
1179
.
Fry
,
F. E. J.
(
1971
).
The effects of environmental factors on the physiology of fish
.
In Fish Physiology
, vol.
6
(ed.
W. S.
Hoar
and
D. J.
Randall
), pp.
1
98
.
New York
:
Academic Press
.
Gallaugher
,
P. E.
(
1994
).
The role of haematocrit in oxygen transport in swimming salmonid fishes
.
PhD thesis
,
Simon Fraser University, Burnaby, British Columbia
.
Gallaugher
,
P.
,
Thorarensen
,
H.
and
Farrell
,
A. P.
(
1995
).
Hematocrit in oxygen transport and swimming in rainbow trout, Oncorhynchus mykiss
.
Respir. Physiol
.
102
,
279
292
.
Gehrke
,
P. C.
,
Fidler
,
L. E.
,
Mense
,
D. C.
and
Randall
,
D. J.
(
1988
).
A respirometer with controlled water quality and computerized data acquisition for experiments with swimming fish
.
Fish Physiol. Biochem
.
8
,
61
66
.
Hochachka
,
P. W.
(
1961
).
The effect of physical training on oxygen debt and glycogen reserves in trout
.
Can. J. Zool
.
3
,
767
776
.
Holmberg
,
B.
and
Saunders
,
R. L.
(
1979
).
The effects of pentachlorophenol on swimming performance and oxygen consumption in the American eel (Anguilla rostrata)
.
Rapp. P.-v. Reun. Cons. int. explor. Mer
.
174
,
144
149
.
Jain
,
K. E.
,
Hamilton
,
J. C.
and
Farrell
,
A. P.
(
1997
).
Use of a ramped velocity test to measure critical swimming speed in rainbow trout (Oncorhynchus mykiss)
.
Comp. Biochem. Physiol
.
117A
,
441
444
.
Jain
,
K. E.
,
Birtwell
,
I. K.
and
Farrell
,
A. P.
(
1998
).
Repeat swimming performance of mature sockeye salmon following a brief recovery period: a sensitive measure of fish health and water quality
.
Can. J. Zool. (in press)
.
Jobling
,
M.
(
1981
).
The influences of feeding on the metabolic rate of fishes: a short review
.
J. Fish Biol
.
18
,
385
400
.
Jones
,
D. R.
(
1971
).
The effect of hypoxia and anaemia on the swimming performance of rainbow trout (Salmo gairdneri)
.
J. exp. Biol
.
55
,
541
551
.
Jones
,
D. R.
(
1981
).
Anaerobic exercise in teleost fish
.
Can. J. Zool
.
60
,
1131
1134
.
Milligan
,
C. L.
and
Wood
,
C. M.
(
1986
).
Tissue intracellular acid–base status and the fate of lactate after exhaustive exercise in rainbow trout
.
J. exp. Biol
.
123
,
123
144
.
Nikl
,
D. L.
and
Farrell
,
A. P.
(
1993
).
Reduced swimming performance and gill structural changes in juvenile salmonids exposed to 2-(thiocyanomethylthio)benzothiazole
.
Aquat. Toxicol
.
27
,
245
263
.
Nrcc
(
1982
).
Chlorinated Phenols: Criteria for Environmental Quality
.
National Research Council of Canada Publication 18578
.
191
pp.
Pagnotta
,
A.
,
Brooks
,
L.
and
Milligan
,
C. L.
(
1994
).
The potential regulatory roles of cortisol in recovery from exhaustive exercise in rainbow trout
.
Can. J. Zool
.
72
,
2136
2146
.
Peake
,
S.
,
Barth
,
C.
and
Mckinley
,
R. S.
(
1997
).
Effect of recovery parameters on critical swimming speed of juvenile rainbow trout (Oncorhynchus mykiss)
.
Can. J. Zool
.
75
,
1724
1727
.
Pearson
,
M. P.
,
Spriet
,
L. L.
and
Stevens
,
E. D.
(
1990
).
Effect of sprint training on swim performance and white muscle metabolism during exercise and recovery in rainbow trout (Salmo gairdneri Richardson)
.
J. exp. Biol
.
149
,
45
60
.
Priede
,
I. G.
and
Young
,
A. H.
(
1977
).
The ultrasonic telemetry of cardiac rhythms of wild free-living brown trout (Salmo trutta L.) as an indicator of bioenergetics and behaviour
.
J. Fish Biol
.
10
,
299
318
.
Randall
,
D. J.
,
Mense
,
D.
and
Boutilier
,
R. G.
(
1987
).
The effects of burst swimming on aerobic swimming in chinook salmon (Oncorhynchus tshawytscha)
.
Mar. Behav. Physiol
.
13
,
77
88
.
Reidy
,
S. P.
,
Nelson
,
J. A.
,
Tang
,
Y.
and
Kerr
,
S. R.
(
1995
).
Post-exercise metabolic rate in Atlantic cod and its dependence upon method of exhaustion
.
J. Fish Biol
.
47
,
377
386
.
Scarabello
,
M.
,
Heigenhauser
,
G. J. F.
and
Wood
,
C. M.
(
1992
).
Gas exchange, metabolite status and excess post-exercise oxygen consumption after repetitive bouts of exhaustive exercise in juvenile rainbow trout
.
J. exp. Biol
.
167
,
155
169
.
Scarabello
,
M.
,
Wood
,
C. M.
and
Heigenhauser
,
G. J. F.
(
1991
).
Glycogen depletion in juvenile rainbow trout as an experimental test of the oxygen debt hypothesis
.
Can. J. Zool
.
69
,
2562
2568
.
Smith
,
L. S.
and
Bell
,
G. R.
(
1964
).
A technique for prolonged blood sampling in free-swimming salmon
.
J. Fish. Res. Bd Can
.
21
,
711
714
.
Soofani
,
N. M.
and
Priede
,
I. G.
(
1985
).
Aerobic metabolic scope and swimming performance in juvenile cod, Gadus morhua L
.
J. Fish Biol
.
26
,
127
138
.
Stevens
,
E. D.
and
Black
,
E. C.
(
1966
).
The effect of intermittent exercise on carbohydrate metabolism in rainbow trout, Salmo gairdneri
.
J. Fish. Res. Bd Can
.
23
,
471
485
.
Thomas
,
R.
and
Rice
,
S. D.
(
1987
).
Effect of water-soluble fraction of Cook Inlet crude oil on swimming performance and plasma cortisol in juvenile coho salmon (Oncorhynchus mykiss)
.
Comp. Biochem. Physiol
.
87C
,
177
180
.
Thorarensen
,
H.
(
1994
).
Gastrointestinal blood flow in chinook salmon (Oncorhynchus tshawytscha
).
PhD thesis
,
Simon Fraser University, Burnaby, British Columbia
.
Thorarensen
,
H.
,
Gallaugher
,
P. E.
,
Kiessling
,
A. K.
and
Farrell
,
A. P.
(
1993
).
Intestinal blood flow in swimming chinook salmon Oncorhynchus tshawytscha and the effects of hematocrit on blood flow distribution
.
J. exp. Biol
.
179
,
115
129
.
Turner
,
J. D.
,
Wood
,
C. M.
and
Clark
,
D.
(
1983
).
Lactate and proton dynamics in the rainbow trout (Salmo gairdneri)
.
J. exp. Biol
.
104
,
247
268
.
Tytler
,
P.
(
1978
).
The influence of swimming performance on the metabolic rate of gadoid fish
.
In Physiology and Behaviour of Marine Organisms
(ed.
D. S.
Mclusky
and
A. J.
Berry
), pp.
83
92
.
Oxford
:
Pergamon Press
.
Waiwood
,
K. G.
and
Beamish
,
F. W. H.
(
1978
).
Effects of copper, pH and hardness on the critical swimming performance of rainbow trout (Salmo gairdneri Richardson)
.
Water Res
.
12
,
611
619
.
Webb
,
P. W.
and
Brett
,
J. R.
(
1973
).
Effects of sublethal concentrations of sodium pentachlorophenate on growth rate, food conversion efficiency and swimming performance in underyearling sockeye salmon (Oncorhynchus nerka)
.
J. Fish. Res. Bd Can
.
30
,
499
507
.
Wood
,
C. M.
(
1991
).
Acid–base and ion balance, metabolism and their interactions after exhaustive exercise in fish
.
J. exp. Biol
.
160
,
285
308
.