Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel

Novel field measurements of critical swimming speed ( U _crit) and oxygen uptake (  M o₂) in three species of adult Pacific salmon Oncorhynchus spp. up to 3·5 kg in body mass were made using two newly designed, mobile Brett-type swim tunnel respirometers sited at a number of field locations in British Columbia, Canada. Measurements of U _crit, which ranged from 1· 68 to 2·17 body lengths s⁻¹, and maximum M o₂, which ranged from 8·74 to 12·63 mg O₂ kg⁻¹ min⁻¹ depending on the species and field location, were judged to be of similar quality when compared with available data for laboratory-based studies. Therefore high quality respirometry studies were possible in the field using adult wild swimming salmonids. In addition, the recovery of wild adult Pacific salmon from the exhaustive U _crit swim test was sufficiently rapid that swimming performance could be repeated with <1 h of recovery time between the termination of the initial swim test and the start of the second test. Moreover, this repeat swimming performance was possible without routine M o₂ being reestablished. This result suggests that wild adult salmon are capable of carrying a moderate excess post-exercise oxygen consumption without adversely affecting U _crit, maximum M o₂ or swimming economy. Such capabilities may be extremely important for timely migratory passages when salmonids face repetitive hydraulic challenges on their upstream migration.     

Swimming performance, oxygen consumption and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched coho salmon

Routine oxygen consumption ( M o ₂) was 35% higher in 1 day starved and 21% higher in 4 day starved adult transgenic coho salmon Oncorhynchus kisutch relative to end of migration ocean-ranched coho salmon. Critical swimming speed ( U _crit) and M o ₂ at U _crit ( M o _2max) were significantly lower in 4 day starved transgenic coho salmon (1·25 BL s⁻¹; 8·79 mg O₂ kg⁻¹ min⁻¹) compared to ocean-ranched coho salmon (1·60 BL s⁻¹; 9·87 mg O₂ kg⁻¹ min⁻¹). Transgenic fish swam energetically less efficiently than ocean-ranched fish, as indicated by a poorer swimming economy at U _crit ( M o _2max     ). Although M o _2max was lower in transgenic coho salmon, the excess post-exercise oxygen consumption (EPOC) measured during the first 20 min of recovery was significantly larger in transgenic coho salmon (44·1 mg O₂ kg⁻¹) compared with ocean-ranched coho salmon (34·2 mg O₂ kg⁻¹), which had a faster rate of recovery.     

Comparisons of swimming performance in rainbow trout using constant acceleration and critical swimming speed tests

Maximum swimming performance of seasonally acclimated rainbow trout Oncorhynchus mykiss was compared among short-duration constant acceleration tests ( U _max) and with the well established, but longer duration critical swimming speed ( U _crit) test. The present results show that U _max was insensitive to a range of acceleration rates that differed by more than three-fold. Thus, test duration could be reduced from 58 to 18 min without affecting the estimate of U _max. The value of U _max, however, was up to 57% higher than U _crit. Only the slowest acceleration rate tested (an increase of 1 cm s⁻¹ every min) had a significantly lower U _max, and this was up to 19% higher than U _crit. Even so, the potential saving in the test duration was small (70 v. 90 min) when compared with a ramp- U _crit test (a standard U _crit test but with the water velocity initially ramped to c . 50% of the estimated U _crit). Therefore, swim tests that are appreciably shorter in duration than a ramp- U _crit test result in U _max being appreciably greater than U _crit. An additional discovery was that the ramp- U _crit performance of cold-acclimated rainbow trout was independent of the recovery period between tests. These results may prove useful in making comparisons among different swim test protocols and in designing swim tests that assess fish health and toxicological impacts.     

The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout

Hatchery cutthroat trout Oncorhynchus clarki clarki were used to examine the effects of 48 h and 3 week temperature acclimation periods on critical swimming speed ( U _crit). The U _crit was determined for fish at acclimation temperatures of 7, 14 and 18° C using two consecutive ramp‐ U _crit tests in mobile Brett‐type swim tunnels. An additional group was tested at the stock's ambient rearing temperature of 10° C. The length of the temperature acclimation period had no significant effect on either the first or the second U _crit( U _crit‐1 and U _crit‐2, respectively) or on the recovery ratio (the quotient of U _crit‐2  U _crit‐1⁻¹). As anticipated, there was a significant positive relationship between U _crit‐1 and temperature ( P  < 0·01) for both acclimation periods, and an increasing, though non‐significant, trend between U _crit‐2 and temperature ( P  = 0·10). Acclimation temperature had no significant effect ( P  = 0·71) on the recovery ratio. These results indicate that a 48 h acclimation to experimental temperatures within the range of −3 to +8° C of the acclimation temperature may be sufficient in studies of swimming performance with this species. This ability to acclimate rapidly is probably adaptive for cutthroat trout and other species that occupy thermally variable environments.     

Coho salmon haematological, metabolic and acid‐base changes during exercise and recovery in sea water

Cannulated, seawater‐acclimated coho salmon Oncorhynchus kisutch were swum to exhaustion in a seawater tunnel (10° C, mean U _crit 50 cm s⁻¹), resulting in metabolic acidosis and increased plasma electrolyte and cortisol concentrations, which were corrected during a 4 h recovery. Because the swimming and physiological performance data were similar to those of other salmonids, it was concluded that life‐history limitations, besides their exercise capabilities in upwelling zones, probably explain declining coho salmon populations.     

Effects of growth hormone transgenesis on metabolic rate, exercise performance and hypoxia tolerance in tilapia hybrids

Swimming respirometry was employed to compare inactive metabolic rate ( R _r), maximum metabolic rate ( R _max), resultant aerobic scope and maximum sustainable (critical) swimming speed ( U _crit), in growth hormone transgenic (GHT) and wild-type (W) tilapia Oreochromis sp. hybrids. Although the R _r of GHT tilapia was significantly (58%) higher than their W conspecifics, there were no significant differences in their net aerobic scope because GHT tilapia exhibited a compensatory increase in R _max that was equal to their net increase in R _r. As a consequence, the two groups had the same U _crit. The GHT and W tilapia also exhibited the same capacity to regulate oxygen uptake during progressive hypoxia, despite the fact that the GHT fish were defending a higher demand for O₂. The results indicate that ectopic expression of GH raises metabolic rate in tilapia, but the fish compensate for this metabolic load and preserve such physiological determinants of fitness as aerobic scope, swimming performance and tolerance of hypoxia.     

Effects of thermal stress on respiratory responses to hypoxia of a South American Prochilodontid fish, Prochilodus scrofa

Oxygen consumption (o₂) and respiratory variables were measured in the Prochilodontid fish, Prochilodus scrofa exposed to graded hypoxia after changes in temperature. The measurements were performed on fish acclimated to 25°C and in four further groups also acclimated to 25°C and then changed to 15, 20, 30 and 35°C. An increase in o₂ occurred with rising temperature, but at each temperature o₂ was kept constant over a wide range of O₂ tensions of inspired water ( Pi o₂). The critical oxygen tensions ( Pc o₂) were Pi o₂= 22 mmHg for 25°C acclimated specimens and after transfer from 25°C to 15, 20, 30 and 35°C the Pc o₂ changed to Pi o₂= 28, 22, 24 and 45 mmHg, respectively. Gill ventilation ( _G ) increased or decreased following the changes in o₂ as the temperature changed and was the result of an accentuated increase in breath frequency. During hypoxia the increases in _G were characterized by larger increases in breath volume. Oxygen extraction was kept almost constant at about 63% regardless of temperature and ambient oxygen tensions in normoxia and moderate hypoxia ( P o₂∼70 mmHg). P. scrofa showed high tolerance to hypoxia after abrupt changes in temperature although its survival upon transfer to 35°C could become limited by the capacity of ventilatory mechanisms to alleviate hypoxic stress.     

Effect of temperature on swimming performance of sea bass juveniles

At four temperatures ( T= 15, 20, 25 and 28° C) swimming performance of Dicentrarchus labrax was significantly correlated with total length (23–43 mm L _T); r²=0.623–0.829). The relative critical swimming speed ( RU _crit= U _crit L _T⁻¹), where U _crit is the critical swimming speed, was constant throughout the L _T range studied. The significant effect of temperature on the relative critical swimming speed was described binomially: RU _crit=−0.0323T²+ 1.578 T −10.588 (r²=1). The estimated maximum RU _crit (8.69 L _T s⁻¹) was achieved at 24.4° C, and the 90% performance level was estimated between 19.3 and 29.6° C.     

Temperature effects on metabolic rate, swimming performance and condition of Pacific cod Gadus macrocephalus Tilesius

Critical swimming speed ( U _crit) and rate of oxygen consumption of Pacific cod Gadus macrocephalus acclimated to 4 and 11° C were determined to assess the influence of water temperature on performance. The physiological effect of exercise trials on fish held at two temperatures was also assessed by comparing haematocrit and plasma concentrations of cortisol, metabolites and ions collected from fish before and after testing. The U _crit of fish acclimated and exercised at 4° C did not differ from those acclimated and exercised at 11° C [1·07 body lengths (total length) s⁻¹]. While the standard metabolic rate of 11° C acclimated fish was 28% higher than that of 4° C fish, no significant difference was observed between fish acclimated at the two temperatures. Plasma concentrations of cortisol, glucose and lactate increased significantly from pre- to post-swim in both groups, yet only concentrations of cortisol differed significantly between temperature treatments. Higher concentrations of cortisol in association with greater osmoregulatory disturbance in animals acclimated at the lower temperature indicate that the lower water temperature acted as an environmental stressor. Lack of significant differences in U _crit between temperature treatments, however, suggests that Pacific cod have robust physiological resilience with respect to swimming performance within temperature changes from 4 to 11° C.     

Gait transition speed as an alternate measure of maximum aerobic capacity in fishes

This study demonstrated that the transition from a steady to an unsteady locomotory gait ( U _STmax) in juvenile brook trout Salvelinus fontinalis can be measured easily using a new tilting raceway design and a simple experimental protocol. It was found that U _STmax increased linearly with fork length ( L _F), and that this relationship was statistically identical in fish that swam volitionally in the raceway and those that were forced to perform, although slightly different data processing methods were needed in the latter to achieve this result. Furthermore, the relationship between L _F and U _STmax was statistically identical to that between L _F and critical swimming speed ( U _crit), although L _F in the former relationship explained 83% of the variance compared to 37% in the latter. This finding indicates that gait transition speed can be used to estimate maximum aerobic capacity, with less unexplainable variance than U _crit. Gait transition speeds were also determined from U _crit tests; however, this required measuring and incorporating ground speed into the analysis. U _STmax as determined in the U _crit tests was not significantly different from that measured in the raceway, suggesting that gait transition speed can be measured in raceways or swim tunnel respirometers.     

Scaling of oxygen consumption of Lake Magadi tilapia, a fish living at 37°C

Rates of oxygen consumption were measured in the geothermal, hot spring fish, Oreochromis alcalicus grahami by stopped flow respirometry. At 37° C, routine oxygen consumption followed the allometric relationship: V o₂=0.738 M ^0.75, where V o₂ is ml O₂ h ⁻¹ and M is body mass (g). This represents a routine metabolic rate for a 10 g fish at 37° C of 0.415 ml O₂ g⁻¹ h ⁻¹ (16.4 μmol O₂ g ⁻¹ h ⁻¹). Acutely increasing the temperature from 37 to 42° C significantly elevated the rate of O₂ consumption from 0.739 to 0.970 ml O₂ g ⁻¹ h ⁻¹ ( Q ₁₀=l.72). In the field, O. a. grahami was observed to be 'gulping' air from the surface of the water especially in hot springs that exceeded 40° C. O. a. grahami may utilize aerial respiration when O₂ requirements are high.     

A reappraisal of activity metabolism in Atlantic cod (Gadus morhua)

Atlantic cod ( Gadus morhua ) were forced to swim in a swim tunnel respirometer until fatigued; oxygen consumption rate (O₂) was measured during swimming at incremental speeds until the fish was exhausted and during recovery from exhaustion. Maximal oxygen consumption (O_2max) occurred during maximal activity as has been found for other fish species, but at odds with the current paradigm for Atlantic cod. Earlier experiments had drawn the conclusion that O_2max in Atlantic cod occurs during recovery from exhaustive exercise. We found no support for this paradigm in our experiments and we propose that the respiratory physiology of Atlantic cod is not unlike that of other fishes.     

Swimming alters responses to hypoxia in the Adriatic sturgeon Acipenser naccarii

When the Adriatic sturgeon Acipenser naccarii was exposed to progressive hypoxia under static conditions, it exhibited a linear decline in O₂ uptake, behaving as an 'oxyconformer'. When, however, it was allowed to swim at a low sustained speed, it could regulate O₂ uptake down to a mean ± s . e . critical ( P _crit) of 4·9 ± 0·5 kPa ( n = 6). At moderate levels of hypoxia, static fish exhibited significant reductions in arterial blood O₂ content, and increases in plasma lactate, which were not observed in swimming animals.     

Reduced swimming abilities in fast-growing transgenic common carp Cyprinus carpio associated with their morphological variations

Critical swimming speeds ( U _crit) and morphological characters were compared between the F₄ generation of GH-transgenic common carp Cyprinus carpio and the non-transgenic controls. Transgenic fish displayed a mean absolute U _crit value 22·3% lower than the controls. Principal component analysis identified variations in body shape, with transgenic fish having significantly deeper head, longer caudal length of the dorsal region, longer standard length ( L _S) and shallower body and caudal region, and shorter caudal length of the ventral region. Swimming speeds were related to the combination of deeper body and caudal region, longer caudal length of the ventral region, shallower head depth, shorter caudal length of dorsal region and L _S. These findings suggest that morphological variations which are poorly suited to produce maximum thrust and minimum drag in GH-transgenic C. carpio may be responsible for their lower swimming abilities in comparison with non-transgenic controls.     

Physiological impact of sea lice on swimming performance of Atlantic salmon

Atlantic salmon Salmo salar were infected with two levels of sea lice Lepeophtheirus salmonis (0·13 ± 0·02 and 0·02 ± 0·00 sea lice g⁻¹). Once sea lice became adults, the ventral aorta of each fish was fitted with a Doppler cuff to measure cardiac output ( ̇ ), heart rate ( f _H) and stroke volume ( V _S) during swimming. Critical swimming speeds ( U _crit) of fish with higher sea lice numbers [2·1 ± 0·1 BL (body lengths) s⁻¹] were significantly lower ( P  < 0·05) than fish with lower numbers (2·4 ± 0·1 BL s⁻¹) and controls (sham infected, 2·6 ± 0·1 BL s⁻¹). After swimming, chloride levels in fish with higher sea lice numbers (184·4 ± 11·3 mmol l⁻¹) increased significantly (54%) from levels at rest and were significantly higher than fish with fewer lice (142·0 ± 3·7 mmol l⁻¹) or control fish (159·5 ± 3·5 mmol l⁻¹). The f _H of fish with more lice was 9% slower than the other two groups at U _crit. This decrease resulted in ̇ not increasing from resting levels. Sublethal infection by sea lice compromised the overall fitness of Atlantic salmon. The level of sea lice infection used in the present study was lower than has previously been reported to be detrimental to wild Atlantic salmon.     

Relationships between heart rate and metabolic rate of pike: integration of existing data

The percentage contribution of heart rate ( f _H) to change in oxygen consumption ( V o₂) was examined in relation to body weight and across the metabolic scope of pike. Also the consequences of variability around the regression relating V o₂ and f _H for estimating V o₂ were considered. The percentage contribution of f _H was calculated using two equations, one that ignored and one that included an estimate for oxygen consumed by the gills and absorbed across the skin ( V o_2s). Using both equations the percentage contribution of f _H calculated using maximum and resting values for f _H and V o₂ decreased with weight of pike. The omission of V o_2s, resulted in erroneously high estimates of the percentage contribution of f _H for pike of any given weight. The omission of V o_2s resulted in erroneously high estimates of the percentage contribution of f _H over the region of the metabolic scope where f _H is related linearly to V o₂, whereas the equation that included V o_2s resulted in the expected value of 100%. Assuming zero experimental error and under normoxic conditions, the 95% confidence limits for single estimates of V o₂ from 30–60-min readings of heart rate are ±39% at a heart rate of 30 beats min ⁻¹. Averaged over longer periods the error decreases, and used over several days to estimate meal size the error is of the order of 1%.     

Respiration of the carp, Cyprinus carpio L., at 10 and 20° C and the effects of hypoxia

Oxygen consumption of carp acclimated at 10 and 20° C has been measured under routine conditions. Some complications and precautions necessary in continuous flow respirometry are discussed. Routine V o₂ at different levels of hypoxia have been determined. Individual variation leads to scatter in the data and different methods of plotting the relationship between V o₂ and P o₂ are proposed; attention is drawn to differences between inlet (or ambient) P o₂ and inspired P o₂. Using certain criteria a 'critical' oxygen tension of about 95 mm Hg was found at 20° C; Q ₁₀ values are about 2 at normoxia and some suggestions of an increase near to the critical oxygen tension were found. Blood samples from the dorsal aorta showed rising Pa,o₂ of 16 mm Hg which increased to 70–80 mm Hg when P _insp was 90 and they then fall as the inspired oxygen is lowered. During periods of deep hypoxia (25 mm Hg) blood lactate concentration increases steadily and indicates an increasing dependence on anaerobic mechanisms.     

Respiratory and acid-base disturbances in rainbow trout blood during exposure to chloramine-T under hypoxia and hyperoxia

Rainbow trout Oncorhynchus mykiss were exposed acutely to chloramine-T at a therapeutic concentration (9mg l⁻¹) under moderately hypoxic (water P o₂: l00 mmHg) or hyperoxic (water P o₂: 430mmHg) conditions and arterial blood gas tensions ( P ao₂ and P aco₂) and pH were monitored using an extracorporeal circulation. Hypoxia, alone, resulted in an increased ventilation frequency, a decrease in both arterial P co₂ and P o₂ and an increase in arterial pH. There was no effect of chloramine-T exposure on the measured variables as compared with pre-exposure (hypoxia baseline) values. Hyperoxia, alone, resulted in a decrease in ventilation frequency, an increase in arterial P co₂ and P o₂, and a decrease in arterial pH. Chloramine-T exposure under these conditions caused a significant increase in ventilation frequency, but no significant effect on arterial blood gases or pH as compared with the hyperoxia baseline values. Despite the increase in ventilation caused by chloramine-T during hyperoxia, there was no reduction in P co₂ or increase in P o₂. Although these results were of little pathological significance, this study suggests that chloramine-T, although stimulating ventilation, was impairing the diffusion of co₂ across the gill probably by the secretion of branchial mucus and enhancing the gill boundary layer.     

Cardiorespiratory status of triploid brown trout during swimming at two acclimation temperatures

At 14° C, standard metabolic rate (75·1 mg O₂ h⁻¹ kg⁻¹), routine metabolic rate (108.8 mg O₂ h⁻¹ kg⁻¹), active metabolic rate ( c . 380 mg O₂ h⁻¹ kg⁻¹), critical swimming speed (U_crit 1·7 BL s⁻¹), heart rate 47 min⁻¹), dorsal aortic pressure (3·2 kPa) and ventilation frequency (63 min⁻¹) for triploid brown trout Salmo trutta were within the ranges reported for diploid brown trout and other salmonids at the same temperature. During prolonged swimming ( c . 80% U _crit), cardiac output increased by 2·3-fold due to increases in heart rate (1·8-fold) and stroke volume (1·2-fold). At 18° C, although standard and routine metabolic rates, as well as resting heart rate and ventilation frequency increased significantly, active metabolic rate and certain cardiorespiratory variables during exercise did not differ from those values for fish acclimated to 14° C. As a result, factorial metabolic scope was reduced (2·93-fold at 18° C v . 5·13-fold at 14° C). Therefore, it is concluded that cardiorespiratory performance in triploid brown trout was not unusual at 18° C, but that reduced factorial metabolic scope may be a contributing factor to the mortality observed in triploid brown trout at temperatures near 18° C.     

Responses of juvenile rainbow trout, under food limitation, to chronic low pH and elevated summer temperatures, alone and in combination

Rainbow trout were exposed (90 days) in synthetic soft water to sublethal low pH (5.2) and a simulated climate warming scenario (+2°C above the control summer temperature range of 16.5–21° C), alone and in combination, under conditions of limited food (∼4% dry body weight day⁻¹). Weight specific oxygen consumption rates ( M o₂) were ∼55% of M o_2(max), in contrast to ∼75% of M o_2(max) found in trout fed an unlimited ration. This is likely due to a reduction in food quantity and thus feeding activity. However, the trout exposed to low pH at control temperatures exhibited higher conversion efficiencies and increased growth. In contrast, trout exposed to +2°C had reduced growth rates. No ionoregulatory disturbance occurred in any treatment, suggesting that this ration was sufficient to provide a replacement salt load in the diet. Energy budgets indicated that the limited ration resulted in a lowered optimum temperature for growth, with a greater proportion of the energy intake dissipated for metabolic expenditure, resulting in reduced conversion efficiencies. A fourfold reduction in faecal and unaccounted energy losses indicated higher absorption efficiencies than in satiation-fed trout.