Influence of seasonal temperature on the repeat swimming performance of rainbow trout Oncorhynchus mykiss
Biological Sciences Department, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada
* Author for correspondence (e-mail: farrell{at}sfu.ca)
Accepted 7 July 2003
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Summary |
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Key words: fish, rainbow trout, Oncorhynchus mykiss, critical swimming speed, temperature acclimation, repeat swimming, plasma, lactate threshold, ammonium
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Introduction |
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A second objective of the present study was to search for correlations
between the ability to reperform after an exhaustive Ucrit
swim and the alteration in plasma levels of ions, metabolites and hormones
during exercise. In particular, possible linkages were sought between the
recovery of swimming performance and the post-exhaustion levels of plasma
potassium, lactate and total ammonia concentrations
(Tamm), all of which have been linked with muscular
exhaustion in both mammals and fish. For example, high intensity exercise in
mammals produces a potassium loss from the muscle
(Sjøgaard et al., 1985;
Vøllestad et al., 1994
;
Hallén, 1996
), which
could decrease the muscle membrane excitability and compromise tension
development (reviewed by Sjøgaard,
1991
). Plasma potassium levels increase in rainbow trout just
prior to Ucrit and, moreover, exercise training increased
Ucrit while blunting and delaying the increases in plasma
potassium and lactate just prior to exhaustion
(Holk and Lykkeboe, 1998
).
Plasma lactate concentration has long been considered a useful indicator of
aerobic limitations and anaerobic capabilities in exercise studies. Indeed,
rainbow trout refused to perform repetitive bouts of burst exercise when
plasma lactate concentration exceeded 13 mmol l-1
(Stevens and Black, 1966
) and
a poorer repeat Ucrit was found for sockeye salmon
Oncorhynchus nerka when plasma lactate concentration was >10 mmol
l-1 (Farrell et al.,
1998
). In mammals, elevated plasma Tamm has
been implicated in exercise fatigue (reviewed by
Mutch and Banister, 1983
) due
to inhibitory influences on anaerobic metabolism
(Zaleski and Bryla, 1977
;
Su and Storey, 1994
), aerobic
metabolism (McKhann and Tower,
1961
; Avillo et al.,
1981
) and neuromuscular coordination
(Binstock and Lecar, 1969
;
O'Neill and O'Donovan, 1979). Plasma Tamm also increases
in rainbow trout during exercise (Turner
et al., 1983
; Wang et al.,
1994
; but see Beaumont et al.,
1995a
,b
).
Furthermore, when routine Tamm was elevated in brown trout
Salmo trutta, as a result of exposure to acidic, copper-containing
water, the subsequent Ucrit performance was inversely
related to pre-exercise plasma Tamm concentration
(Beaumont et al., 1995a
). Thus,
because plasma levels of potassium, lactate and Tamm are
good indicators of exhaustion in fish, we anticipated that they are
potentially strong indicators of repeat swimming capability in rainbow trout.
If this is the case, the expectation is that individual variation in these
plasma variables prior to a second swim would be correlated with individual
variation in the performance of a second Ucrit test
compared to the initial performance.
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Materials and methods |
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Swim tunnel
Fish were swum in a modified Brett-type swim tunnel, similar to that
described by Gehrke et al.
(1990). The swim chamber was
21 cm diameter and 97 cm length, with a metal grid at each end. The rear grid
was equipped with an electrical pulse generator (4 V) that, when contacted by
the fish, provided a mild stimulation to encourage the fish to swim forward.
Water speed was uniform across the swim tunnel throughout the speed range used
in these experiments. The water current in the tunnel was produced by a
3-phase induction motor and a centrifugal pump attached to a tachometer whose
readings (Hz) were calibrated with known water velocities, as measured with a
Valeport current meter (Valeport Marine Scientific Ltd., Dartmouth, UK).
Protocol for arterial cannulation
The dorsal aorta was cannulated to permit sampling of blood prior to and
during the swimming tests, and during the recovery periods. Arterial
cannulation was performed under anesthesia (0.1 g l-1 buffered
MS-222; Syndel Laboratories, Vancouver, BC, Canada), using the method of Smith
and Bell (1964). Fish mass,
fork length, maximum width and maximum depth were also measured at this time.
Cannulated fish were either placed in the swim tunnel to recover or returned
to the outdoor tank, where they recovered for up to 3 days before being placed
in the swim tunnel. During subsequent transfer from the outdoor tank to the
tunnel, fish were lightly and briefly anaesthetized (0.05 g l-1
buffered MS-222). There was no significant relationship between
post-cannulation recovery time and measured swimming performance (data not
presented).
Habituation to the swim tunnel and high water velocities
Fish recovered from anesthesia in the tunnel at a water speed of 10 cm
s-1 for at least 45 min. After this time, fish performed a 20 min
practice swim, as suggested in Jain et al.
(1997), during which water
speed was increased in 9-10 cm s-1 increments every 2 min to a
speed of
41 cm s-1. Water speed was then returned to 10 cm
s-1 for 2 min and again increased in the same fashion to a speed of
either 55 or 59 cm s-1, depending on the fish's swimming
capability. The practice swim, which did not exhaust the fish, prevented the
training effect often observed with naive fish on a second
Ucrit (Farlinger and
Beamish, 1977
; Jain et al.,
1997
). Fish then recovered overnight (14-16 h) at a water speed of
10 cm s-1.
Swimming protocol
All experiments were started between 08:00 h and 10:00 h. Fish performed a
ramp-Ucrit test (Jain
et al., 1997). The first Ucrit test was
followed by a 40 min recovery period at a water speed of 10 cm s-1
and then a second ramp-Ucrit test followed by another
recovery period. Each ramp-Ucrit test involved increasing
water speed to
50% of Ucrit over a 5 min period,
after which water speed was increased in 10 cm s-1 increments
(
15% of Ucrit) every 20 min until exhaustion.
Exhaustion was taken as the point at which the fish failed to swim away from
the electrified rear grid after 20 s of contact. The
ramp-Ucrit protocol produces similar values for
Ucrit to the more standard Ucrit
testing protocol in which the longer time intervals are used from the onset of
the test (Jain et al.,
1997
).
Ucrit values were calculated for the first
(Ucrit1) and second (Ucrit2) swims, as
described by Brett (1964):
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Blood sampling
Blood samples (0.9 ml) were taken through the dorsal aorta cannula to
measure plasma ion and metabolite levels. Normally, samples were taken
immediately prior to the swimming protocol (routine samples), at exhaustion
for both swim tests (Ucrit exhaustion samples), and after
a 40 minrecovery for both tests (recovery samples; the recovery sample for the
first Ucrit swim also served as the sample taken
immediately before the second Ucrit swim). In 14 of the 16
fish, a blood sample was taken during aerobic swimming, i.e. after 15 min at
45 cm s-1 (approx. 69% Ucrit). (These data are
not reported as they simply provided intermediate values between the routine
and Ucrit values.) An equal volume of physiological saline
solution was used to replace all blood samples
(Gallaugher et al., 1992).
Routine hematocrit was never less than 23% and remained elevated throughout
the swim tests (see Fig.
2D).
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Analytical techniques
Hematocrit was measured in microcapillary tubes after centrifugation at
2000 g for 3 min. The remainder of the blood was centrifuged
at 10 000 g for 5 min to obtain plasma, which was stored at
-80°C. Within 1 week of testing, plasma lactate and glucose concentrations
were measured on 25 µl samples using a YSI 2300 lactate/glucose analyzer
(Yellow Springs, OH, USA) that calibrated automatically every five samples.
Plasma potassium and sodium concentrations were measured using a model 510
Turner flame photometer (Palo Alto, CA, USA). Plasma (5 µl) was diluted
1:200 with a prepared 15 mEq l-1 lithium diluent for analysis. The
machine was calibrated prior to use and checked against a standard
approximately every six samples. The measurement was repeated if there was
disagreement between duplicates beyond 2% of absolute value. Osmolality was
measured on duplicate 10 µl samples using a calibrated Wescor Vapour
Pressure Osmometer, Model 5500 (Wescor, Logan, UT, USA). The measurement was
repeated if there was disagreement between duplicates beyond 3% of absolute
value. The thermocouple heads were cleaned periodically in order to maintain
consistency. Plasma cortisol concentration was measured using a commercial
radioammunoassay kit (ICN Biomedicals, Inc., Costa Mesa, CA, USA), with a
detection limit of 1.5 ng ml-1. Plasma ammonia concentration
(Tamm) was measured spectrophotometrically on 0.1 ml
plasma samples (Sigma Diagnostics kit no. 171, St Louis, MI, USA) with a
calibration every seven samples.
Data analysis
All plasma metabolites and ions were measured in duplicate and averaged for
individual data. Fish were subdivided into two temperature acclimation groups
based on their swimming performance (see Results) and values (mean ±
S.E.M.) are presented for cold- and warm-acclimated fish. One
warm-acclimated female fish that was overtly gravid was not included in the
statistical analysis to eliminate any confounding effect, because reproductive
maturity is known to negatively affect Ucrit performance
in salmon (Williams et al.,
1986). Statistical comparisons within temperature groups were made
with a one-way repeated measures analysis of variance (ANOVA) followed by a
post hoc Tukey test. With this test, the values associated with each
fish were compared to other levels at other sampling times for the same fish
to determine whether either swimming speed or metabolite levels changed
throughout testing. Comparisons of swimming performance and metabolite levels
between temperature groups were made using t-tests.
Ucrit1 was compared to Ucrit2 using a
Bland-Altman plot. Bland and Altman
(1986
,
1995
) introduced this method of
graphical analysis to assess the equivalency of two testing approaches (here
Ucrit1 and Ucrit2), while removing the
bias that comes from assuming that one method represents the true value
(independent variable). The Bland-Altman plot uses the mean of both methods as
the independent variable and the difference between the two testing methods as
the dependent variable. If the linear regression of the points is
non-significant, then the two testing procedures (i.e.
Ucrit1 and Ucrit2 here) can be
considered to be equivalent testing procedures. Sub-groups can be identified
within a data set in a Bland-Altman plot by demonstrating different
significant linear regressions from each other. In the present study,
different regressions would identify sub-groups with different relationships
between Ucrit1 and Ucrit2.
Relationships between Ucrit values and plasma variables
were fitted with the best-fitting regressions using the options provided in
Sigma-Plot (SPSS Inc.; Chicago, IL, USA). P<0.05 was used to
establish statistical significance.
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Results |
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A Bland-Altman plot revealed that Ucrit1 and Ucrit2 were equivalent testing procedures (P=0.98), but visual inspection of the plot revealed that overall the fish could be divided into two sub-groups each with a different and significant linear relationship (Fig. 1A). Each of the two sub-groups corresponded to different acclimation temperatures and hereafter are termed warm- and cold-acclimated fish (14.9±1.0°C and 8.4±0.9°C, respectively; see Table 1).
|
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Ucrit1 performance was temperature dependent (Fig. 1B;r2=0.74, P<0.05). Ucrit1 (78.9±1.0 cm s-1) for warm-acclimated fish was significantly greater (P<0.05) than that for cold-acclimated fish (59.1±2.5 cm s-1; Table 1). However, Ucrit2 did not show any temperature dependency. Unexpectedly, Ucrit2 performance (65.8±2.70 cm s-1) for warm-acclimated fish was significantly lower than Ucrit1, whereas Ucrit2 for cold-acclimated fish (58.0±4.2 cm s-1) was the same as their Ucrit1 values (Table 1). As a result, the overall relationship between Ucrit1 and Ucrit2 was best described by a polynomial equation (y=-204.3+7.57x-0.05x2; P<0.001; Fig. 1C), with cold-acclimated fish lying close to the line of identity and warm-acclimated fish lying below the line of identity. Thus, while warm acclimation conferred a faster Ucrit1, a similar swimming speed could not be attained after a 40 min recovery period, as shown by recovery ratios that are less than unity for warm-acclimated fish (Fig. 1D).
Plasma status before, during and after
Ucrit tests
There were no significant differences between the cold- and warm-acclimated
groups of fish in terms of routine values for plasma levels of lactate,
potassium, Tamm, sodium, glucose, cortisol and osmolality
and hematocrit. When cold-acclimated fish were exhausted at
Ucrit1, plasma levels of lactate, potassium and
Tamm, as well as hematocrit, all increased significantly
(Fig. 2A-D). Plasma cortisol
(Fig. 2E) and sodium
(Fig. 2F) levels were unchanged
at exhaustion for Ucrit1. After a 40 min recovery from
Ucrit1, plasma lactate increased significantly beyond the
level observed at exhaustion, plasma Tamm decreased to the
routine level, and plasma potassium and hematocrit remained elevated at the
same level. As a result, plasma lactate and potassium levels, and hematocrit
were all significantly elevated at the outset of the
Ucrit2 test.
For cold-acclimated fish exhausted at Ucrit2, plasma levels of lactate, potassium, sodium and Tamm, and hematocrit, were again significantly elevated compared with the routine values, but no more so than for Ucrit1. In fact, compared with the recovery values for Ucrit1, plasma lactate levels had decreased significantly (Fig. 2A) at exhaustion for Ucrit2, while Tamm had increased significantly (Fig. 2C). Similar to Ucrit1, plasma lactate increased during the 40 min recovery from Ucrit2 to a level significantly higher than that observed at exhaustion, plasma Tamm decreased to the routine level, and plasma potassium and hematocrit remained elevated at the same level. As a result, none of the recovery values for Ucrit2 in cold-acclimated fish were significantly different to those for Ucrit1. Plasma levels of cortisol, glucose and osmolality remained unchanged throughout both swimming protocols (data not shown). Therefore, the second swim for cold-acclimated fish had no additive effects on any of the measured plasma variables.
When warm-acclimated fish were exhausted at Ucrit1, plasma Tamm and hematocrit increased by the same amount as for cold-acclimated fish (Fig. 2C,D). In contrast, the faster Ucrit1 of the warm-acclimated fish was associated with significantly larger increases in plasma levels of lactate and potassium (Fig. 2A,B) compared with cold-acclimated fish. Furthermore, warm-acclimated fish significantly increased plasma sodium and cortisol levels at exhaustion for Ucrit1 (Fig. 2E,F), unlike cold-acclimated fish. After a 40 min recovery from Ucrit1, the levels of plasma lactate, potassium, Tamm, sodium and cortisol, as well as hematocrit all remained significantly elevated in warm-acclimated fish, whereas only plasma levels of lactate, potassium and hematocrit remained elevated in cold-acclimated fish (Fig. 2). In addition, plasma lactate, potassium, sodium and cortisol remained elevated in warm-acclimated fish at levels that were significantly greater than those observed in cold-acclimated fish during recovery. In fact, the plasma lactate level was about threefold higher and plasma potassium almost twofold higher. These results suggest that the higher Ucrit1 of warm-acclimated fish may have been partly due to a greater anaerobic swimming effort compared with cold-acclimated fish, and (or) lactate and potassium were released from muscle to plasma to a greater extent.
Compared with cold-acclimated fish, warm-acclimated fish clearly began the second Ucrit test with a greater plasma ionic and metabolic disruption and, as a result in these fish, Ucrit2 was significantly lower than Ucrit1. In addition, while Ucrit2 for warm-acclimated and cold-acclimated fish was the same, warm-acclimated fish displayed a significant, further increase in plasma potassium levels (Fig. 2B) at exhaustion and a significant, further increase in plasma lactate levels (Fig. 2A) during the recovery from Ucrit2. However, plasma Tamm did not recover to a routine level, as it did in the cold-acclimated fish (Fig. 2C). Therefore, the second Ucrit swim of warm-acclimated fish produced significant additive effects on some of the plasma variables, unlike in cold-acclimated fish where there were none.
Correlational analysis
The initial swimming performance of individual fish was related to the
appearance of lactate in the plasma. Plasma lactate concentrations measured at
Ucrit1 and after a 40 min recovery were both linearly
related to Ucrit1 (Fig.
3; r2=0.73, P<0.05 and
r2=0.79, P<0.05, respectively). As might be
expected from Fig. 3, plasma
lactate concentrations were highly correlated with each other (2nd
exhaustion with 1st exhaustion: r2=0.95,
P<0.05; 1st exhaustion with 1st recovery:
r2=0.92, P<0.05; 2nd exhaustion
with 1st recovery: r2=0.94, P<0.05;
2nd recovery with 2nd exhaustion:
r2=0.94, P<0.05).
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The difference in swimming performance between Ucrit1 and Ucrit2 was significantly related to the plasma lactate concentration prior to the second Ucrit test (Fig. 4). This relationship was described by either a polynomial (r2=0.74), or a 2-parameter power (r2=0.65) regression. Both types of analysis suggest that the reduction in Ucrit2 relative to Ucrit1 occurred when fish reached a plasma lactate of 12.2 mmol l-1 (95% confidence intervals of 7.9 and 16.5 mmol l-1) 40 min after being exhausted by an initial Ucrit swim test. Only warm-acclimated fish reached this threshold plasma lactate level.
|
Swimming effort in the initial swim was also related to the appearance of potassium in the blood. Plasma potassium concentration measured at Ucrit1 was linearly related to Ucrit1 (r2=0.60, P<0.05). However, there was no significant correlation between plasma potassium levels and performance on the second swim. Plasma Tamm at exhaustion was not significantly related to Ucrit1, but Tamm values for the 1st recovery were related to Ucrit1 (Fig. 5; r2=0.34, P<0.05). There were no other significant correlations for plasma Tamm.
|
The influence of acclimation temperature on the plasma ionic and metabolic responses to exercise is illustrated by the significant linear correlations that existed between plasma lactate, cortisol and potassium levels and temperature (Table 2). There were no significant correlations with temperature and the other parameters measured (Tamm, [sodium] and hematocrit).
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One overtly gravid, warm-acclimated female fish was treated as an outlier, based on its slow swimming performance, and was not used for any correlation analysis. However, it is important to note that all the plasma changes observed in this fish were consistent with the slower swimming performance of the cold-acclimated fish.
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Discussion |
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Our original hypothesis, which we now reject, was based on the established
temperature dependence of post-exercise metabolic and ionic recovery when
salmonids are chased to exhaustion to produce similar levels of intracellular
acidosis, lactate accumulation and glycogen depletion in white muscle
regardless of temperature (Kieffer et al.,
1994; Wilkie et al.,
1997
). However, when Atlantic salmon were angled to exhaustion at
a warmer temperature, essentially the opposite effect of temperature on
post-exercise muscle recovery was obtained; they displayed a greater depletion
of muscle glycogen, a greater intracellular acidosis and a slower recovery of
muscle metabolites at the warmer temperature compared with colder temperatures
(Booth et al., 1995
;
Wilkie et al., 1996
). The
present findings for Ucrit swim tests are more in line
with data obtained when fish are angled rather than chased to exhaustion
because the metabolic disturbances were higher and performance recovery slower
at warmer temperatures. We suggest that the disparity among studies could
simply reflect differences in the degree of exhaustion and the methods used to
exhaust the fish, with fish becoming more exhausted because they perceive the
chasing protocol as more of a threat or provocation than either angling or
Ucrit testing. Given this possibility, cold-acclimated
fish could opt to stop swimming sooner than warm-acclimated fish to preserve
glycogen reserves.
A Ucrit value, like time-to-exhaustion at a prescribed
water speed (e.g. Facey and Grossman,
1990; Mitton and McDonald,
1993
), allows quantification of the swimming effort, something
that is not easily done when fish are chased or angled to exhaustion.
Ucrit tests also encompass a spectrum of swimming speeds,
with the aerobic demands of swimming up to maximum oxygen uptake being met by
cardiorespiratory adjustments, while white muscle recruitment and anaerobic
metabolism increasingly supports the higher muscular power output near
Ucrit (Burgetz et al.,
1998
), culminating in exhaustion
(Brett, 1964
;
Beamish, 1978
). The simplest
explanation for the higher Ucrit1 values obtained for
warm-acclimated compared with cold-acclimated fish is a greater involvement of
anaerobic swimming, given the significantly larger alterations in plasma
metabolites observed for warm-acclimated rainbow trout. Certainly, the
warm-acclimated fish were more stressed than the cold-acclimated fish, as
judged by the greater elevation in plasma cortisol levels. However, since
muscle metabolites were not measured here, we cannot exclude other
possibilities. The higher levels of plasma potassium, lactate and
Tamm, as well as the additive effects of the second swim,
could simply reflect a greater release of lactate and potassium into the
plasma because the release of lactate and hydrogen ions from white muscle to
the blood is known to be temperature dependent (see
Kieffer, 2000
). Nevertheless,
it is unlikely that different muscle glycogen levels were a factor since these
are unaffected by acclimation temperature
(Kieffer, 2000
).
Rome et al. (1985) showed
that acutely exposing warm-acclimated carp Cyprinus carpio to cold
water resulted in white muscle fibres being recruited at a lower swimming
speed, and this `compression of recruitment order' led to earlier fatigue and
a reduced sustained swimming speed. However, when the carp were
cold-acclimated, they recruited white muscle at a higher swimming speed than
warm-acclimated fish, presumably because cold temperature acclimation had
improved the mechanical performance of the red muscle. The present findings
are consistent with this earlier work with carp in that the cold-acclimated
rainbow trout appeared to rely less on anaerobic white muscle than
warm-acclimated fish, but the two studies differ in that cold-acclimated
rainbow trout had a lower Ucrit than warm-acclimated
rainbow trout whereas cold-acclimated carp swam to the same maximum speed as
warm-acclimated fish (Rome et al.,
1985
). Rome et al.
(1985
) suggested three
possible physiological differences in cold-acclimated fish compared with
warm-acclimated fish: (1) a higher mechanical power output from aerobic
muscle, (2) limitations on the neural control of locomotory muscle and (3)
limitations of the respiratory and circulatory systems in supplying oxygen.
The present findings suggest a fourth possibility: fish may opt to swim to
different states of exhaustion depending on either the temperature or a
resulting physiological condition. One benefit of limiting the level of
exhaustion under cold conditions appears to be a more reasonable recovery
rate, which allows for repeated performance. At warm temperatures, fish
benefit from a higher initial level of performance but, by exhausting
themselves to a relatively greater degree, have the disadvantage of a more
prolonged recovery period. An additional disadvantage, but for unknown
reasons, is that exhaustive exercise at warm, but not at cold temperatures,
can result in appreciable levels of postexercise mortality (see
Kieffer, 2000
).
The present conclusions are also in line with the results of McKenzie et
al. (1996) working with Nile
tilapia Oreochromis nilotica. They found that
warm-acclimated fish had a greater cost of recovery (a higher and more
prolonged post-exercise oxygen consumption) after being chased to exhaustion
than cold-acclimated fish. Interestingly, white muscle lactate accumulation
was similar for 16°C-acclimated and 23°C-acclimated tilapia,
suggesting that muscle lactate may not always be a reliable measure of
post-exercise recovery. However, 23°C-acclimated tilapia excreted over
twice the amount of ammonia post-exercise than 16°C-acclimated fish.
Kieffer et al. (1998
)
similarly found that ammonia excretion at 75% Ucrit was
almost threefold higher for 15°C-acclimated than 5°C-acclimated
rainbow trout, while protein utilization at 75% Ucrit was
30% at 15°C versus 15% at 5°C. Likewise, in the present
study, we observed a significantly higher plasma Tamm in
warm-acclimated rainbow trout. As discussed by McKenzie et al.
(1996
), the elevated ammonia
production could be a result of either increased protein metabolism to fuel
locomotion or increased protein degradation from tissue damage. Since elevated
Tamm is thought to have inhibitory actions on neural and
muscle activity in fish (Beamount et al., 1995a), the larger elevation in
plasma Tamm in warm-acclimated fish is perhaps critical to
survival post-exhaustion. On the other hand, tissue damage might negatively
affect Ucrit2.
Ucrit values were comparable to those reported earlier
by Jain et al. (1997) for
rainbow trout of the same size in the same swim tunnel [1.64-1.66 body lengths
(BL) s-1] and higher than those reported for 822-1118 g
rainbow trout (0.94 BL s-1 and 0.53 BLs-1 at 11°C and 18°C, respectively;
Taylor et al., 1996
).
Comparisons also can be made with studies on smaller rainbow trout, which are
expected to attain slightly higher Ucrit values
(Brett, 1964
) than the 879 g
fish used here. Ucrit values of 1.8 to 2.0 BLs-1 are reported for 530-730 g rainbow trout at 18-19°C
(Gallaugher et al., 1992
) and
2.13 BL s-1 for 431-483 g rainbow trout at 7-11°C
(Burgetz et al., 1998
). For
320-520 g brown trout, Ucrit values were 2.2 BLs-1 at 15°C and 1.85 BL s-1 at 5°C
(Butler and Day, 1993
;
Butler et al., 1992
).
As anticipated, a 40 min recovery period allowed full recovery of swimming
performance for cold-acclimated fish. Originally it was suggested that
salmonids be given 4 hbetween Ucrit tests
(Brett, 1964) to ensure a
return to routine O2 consumption but not necessarily to routine
glycogen levels. Subsequently, recovery times of 2 h
(Brauner et al., 1994
), 1 h
(Randall et al., 1987
), 45 min
(Farrell et al., 1998
,
2003
) and 40 min
(Jain et al., 1998
) have all
been shown to be sufficient for salmonids to repeat Ucrit
tests without any significant decline in performance. Here fish were provided
with a low speed water current during recovery and this may have aided their
recovery, since recent studies with rainbow trout
(Milligan et al., 2000
) and
coho salmon Oncorhynchus kisutch
(Farrell et al., 2001
) have
shown that low to moderate swimming post-exhaustion greatly aids metabolic
recovery through a warm-down effect. In contrast, recovery time without a
warm-down is >2 h for optimal performance on a time-to-exhaustion test
(Mitton and McDonald, 1994). Wang et al.
(1994
) reported that muscle
phosphocreatine and ATP levels were restored within 30 min of rainbow trout
being chased to exhaustion, while the post-exercise decline of oxygen
consumption lasted 3-3.5 h (Scarabello et
al., 1991
). However, routine oxygen consumption does not have to
be restored before adult sockeye salmon can repeat a second
Ucrit test (Farrell et al.,
1998
,
2003
).
There was generally good agreement between the routine plasma variables
reported here and those reported in previous studies
(Butler and Day, 1993;
Eros and Milligan, 1996
;
Pagnotta et al., 1994
;
Thorarensen et al., 1994; Wang et al.,
1994
). However, the plasma lactate concentrations at
Ucrit in this study, especially those for the
warm-acclimated fish (7.3 mmol l-1), were at the high end of
literature values for Ucrit swimming (1.5-5.5 mmol
l-1) (Butler and Day,
1993
; Gallaugher et al.,
1992
; Thorarensen et al.,
1993
; Holk and Lykkeboe,
1998
; Farrell et al.,
1998
). Milligan
(1996
) cites a range for
plasma lactate levels of 2-13 mmol l-1 immediately after chasing,
increasing to peak values of 12-20 mmol l-1 at 2 h post-exercise.
The values reported here for cold-acclimated fish of 4.3 mmol l-1
at Ucrit and 8.9 mmol l-1 40 min later are at
the low end of this range, whereas those for the warm-acclimated fish (7.3
mmol l-1 at Ucrit and 16.6 mmol l-1
40 min later) are at the upper end of the range and approached the level
reached (17.8 mmol l-1) approximately 90 min after a hypoxic
Ucrit test (Farrell et
al., 1998
).
The second objective of the present study was to determine whether any of
the measured metabolites displayed threshold levels that, if surpassed in the
first swim challenge, were indicative of a metabolic condition that negatively
affected subsequent swimming performance. Plasma lactate level was the only
candidate: the plasma lactate level before Ucrit2 was
significantly correlated to the subsequent swimming performance
(Ucrit2). The threshold plasma lactate level of
approximately 12.2 mmol l-1 (95% CI 7.9-16.4) agrees with that of
13 mmol l-1 reported by Stevens and Black
(1966) for burst exercise with
rainbow trout and 10 mmol l-1 for sockeye salmon
(Farrell et al., 1998
). In the
earlier studies, fish refused to swim if the lactate threshold was surpassed.
However, no fish refused to swim outright in the present study and instead
Ucrit performance was reduced by 8-31%. Thus, because
anaerobic metabolism is increasingly required to support swimming speeds
greater than 70% Ucrit
(Burgetz et al., 1998
),
elevated levels of lactate above the lactate threshold is probably indicative
of a failure to fully recruit anaerobic metabolism in white muscle (e.g.
through decreased muscle pH and glycogen stores). This idea needs further
study, however, because plasma lactate dynamics are complex, reflecting rates
of production in the muscle, rates of release from the muscle and rates of
clearance from the blood. While the present study suggests that production may
be greater at warmer temperatures, release rate is dependent on temperature
(Keiffer et al., 1994) and clearance rate is inversely related to temperature
(Kieffer and Tufts, 1996
).
Beaumont et al.
(1995a,b
)
reported that copper-exposed brown trout in water of low pH had poor
Ucrit values and suggested that the elevated plasma
Tamm inhibited white muscle activity either directly or
through CNS inhibitory mechanisms, because elevated plasma
Tamm levels were correlated with the reduced
Ucrit values. In the present study, we found no
significant correlations between swimming performance and plasma
Tamm. However, our data are not necessarily at odds with
the suggestion of Beaumont et al.,
(1995a
,b
)
because the plasma Tamm levels reported in the present
work were half those measured in copper-exposed brown trout and, in the
earlier studies, Ucrit was not reduced appreciably until
plasma Tamm reached levels >200 µmol l-1.
A plasma Tamm level >600 µmol l-1
resulted in fish refusing to swim. In the present study,
Tamm reached only 100 µmol l-1 and was
restored between Ucrit tests for cold-acclimated fish,
although not for warm-acclimated fish (Fig.
2).
Several studies report a temperature optimum for Ucrit.
For sockeye salmon, 15°C was the optimum temperature for
Ucrit, metabolic scope
(Brett, 1964) and cardiac
performance (Brett, 1971
;
Davis, 1968
). The preferred
temperature for sockeye salmon, however, appears to be slightly cooler
(10-12°C; Birtwell et al.,
1994
; Spohn et al.,
1996
). Garside and Tait
(1958
) suggested a preferred
temperature range for rainbow trout of 11-16°C, which coincides with the
optimum temperature range suggested for cardiac performance
(Farrell et al., 1996
;
Taylor et al., 1997
;
Farrell, 2002
). The present
experiments show that the shift in responses to repeated swimming for cold-
and warm-acclimated fish occurred at around 12°C. Therefore, the fish's
preferred temperature may reflect sub-maximal rates for certain activities
because of negative consequences in terms of rates of recovery.
In summary, we provide evidence that warm-acclimated rainbow trout have a higher Ucrit than cold-acclimated fish, but associated with this higher Ucrit is a greater metabolic and ionic disturbance. A consequence of this elevated disturbance is that warm-acclimated fish do not recover well enough after a 40 min rest to perform a second test at the same level as the first one, whereas cold-acclimated fish do. Elevations in plasma lactate (but not plasma potassium, Tamm and cortisol) were significantly correlated with the poorer repeat swimming performance.
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