Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming
1 Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6,
Canada
2 Department of Forest Sciences, University of British Columbia, Vancouver,
BC, V6T 1Z4, Canada
3 Institute for Resources and Environment, University of British Columbia,
Vancouver, BC, V6T 1Z4, Canada
* Author for correspondence (e-mail: Farrell{at}sfu.ca)
Accepted 18 June 2003
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Summary |
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Key words: recovery, exhaustive exercise, salmon, oxygen consumption, non-aerobic swimming, post-exercise oxygen cost (EPOC), fish stock, spawning run
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Introduction |
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The elevated
O2 following
exhaustive exercise, termed `excess post-exercise oxygen consumption' (EPOC;
Gaesser and Brooks, 1984
) can
be used to assess both recovery time and the non-aerobic oxygen cost of
exercise. EPOC, which replaces the term `oxygen debt'
(Hill et al., 1924
) to avoid
causal implications, reflects the increased quantity of oxygen required to
restore tissue and cellular stores of oxygen and high-energy phosphates,
biochemical imbalances in metabolites such as lactate and glycogen, and other
functions such as ionic and osmotic balance. Measurements of EPOC with
salmonids are limited, however, to juvenile, hatchery-raised fish. In fact,
the number of studies of EPOC in all ectotherms is quite limited (e.g.
Heath and Prichard, 1962
;
Brett, 1964
;
Smit, 1965
;
Smit et al., 1971
; Scarabello
et al., 1991
,
1992
;
Gleeson, 1991
;
Reidy et al., 1995
;
Hancock et al., 2001
) compared
with mammals (e.g. Bahrm and Maehlum,
1986
; Bangsbo et al.,
1997
; Baker and Gleeson,
1998
).
The pioneering measurements of EPOC following a Ucrit
test with juvenile, hatchery-reared sockeye revealed that
O2 returned to a
routine level after 4-5 h (Brett,
1964
). A similarly protracted recovery time of up to 6 h was
reported for juvenile, hatchery-reared rainbow trout O. mykiss after
vigorous chasing for 3 min followed by an electrical stimulation for a further
2 min (Scarabello et al.,
1992
). In contrast, recovery time was only 1.5 h in adult Atlantic
cod Gadus morhua, regardless of whether the fish had been chased to
exhaustion, accelerated to exhaustion, or performed a
Ucrit test (Reidy et
al., 1995
). Furthermore, the protracted recovery times for
juvenile salmonids contrasts with their ability either to repeat
Ucrit after as little as a 45 min recovery period
(Randall et al., 1987
;
Peake et al., 1997
;
Jain et al., 1997
; Farrell et
al., 1998
,
2003
), or to repeat burst
swimming 60 min after being chased, swum or fished to exhaustion
(Stevens and Black, 1966
;
Farrell et al., 2001b
).
Although none of these studies measured EPOC along with repeat swimming
performance,
O2
for adult, wild sockeye salmon did approach routine
O2 after only a
45 min recovery period (Farrell et al.,
1998
). Given the possibility of a difference in recovery times
between juvenile and adult salmonids, the present study measured post-exercise
O2 for adult,
wild salmon during recovery from exhaustion following a
Ucrit test. Because EPOC was measured concurrently with
the accompanying assessment of swimming energetics on various salmon stocks
(Lee et al., 2003
) that
encounter different ambient water temperatures and hydraulic challenges while
migrating up the Fraser River to different natal streams, we sought additional
information on some of the other factors that may modulate EPOC, none of which
have been thoroughly studied in fish.
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Materials and methods |
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Exercise protocols
Prior to an overnight recovery in the swim tunnel at a water speed of
0.30-0.45 body lengths (BL) s-1, fish were given a
practice swim (Jain et al.,
1997) to estimate Ucrit. The following
morning, routine
O2
(
O2routine) was
measured over a period of 15-20 min. Then a ramp-Ucrit
test (Jain et al., 1997
) was
performed using the 471 litre mobile swim tunnel respirometer. Initially, 5
min ramp steps of 0.15 BL s-1 were used up to 50% of the
estimated Ucrit, followed by 20 min steps of 0.15
BL s-1 until Ucrit. As fish approached
their Ucrit, a burst-and-coast swimming gait was used more
frequently, and this change in swimming gait was associated with progressive
accumulation of lactate in the white skeletal muscle
(Burgetz et al., 1998
).
O2 was measured
at every other speed increment, and the
O2 measured
immediately before Ucrit was designated maximum
O2
(
O2max). Fish
were considered exhausted when they failed to move off the rear grid after 20
s, at which time water speed was immediately decreased to between 0.30 and
0.45 BL s-1 for the 45 min recovery period during which
EPOC was measured. In most cases, the swim tunnel was closed for the entire
recovery period and
O2 was estimated
at 5 min intervals. Water oxygen concentration would typically decrease by
1.5-2.5 mg O2 l-1 to a final water concentration of
approximately 8.0 mg O2 l-1. In a few instances (large
fish at a warm temperature), the water oxygen concentration approached 6.0 mg
O2 l-1 and so the swim tunnel was flushed with fresh
water for up to 5 min, with the resultant loss of that
O2 measurement.
When
O2 was not
being measured, water flow into the swim tunnel was restored. The
ramp-Ucrit protocol was repeated after this recovery
period and EPOC was remeasured after the fish fatigued for a second time.
Data analysis and statistics
Values are means ± S.E.M. and P<0.05 was used
as the level of statistical significance. For reference,
O2routine,
O2max and
Ucrit (as reported in
Lee et al., 2003
) are
summarized in Table 1. These
values were based on an average value for the first and second swim tests
because the two swim tests were not significantly different. EPOC values were
treated in the same manner. The present analysis of recovery time and
non-aerobic cost of swimming was based on the relationship between mean
O2 and time
during the Ucrit swim test and recovery period (as
presented in Fig. 1). For
regression analysis of mean
O2 values
versus time after exhaustion (SigmaPlot 6.0, SPSS, Chicago, IL, USA),
it was assumed that
O2 decayed
exponentially during recovery (Brett and
Groves, 1979
; Scarabello et
al., 1991
). Total EPOC (mg O2 kg-1) was
obtained by integrating (Maple 8.00, Waterloo Maple Inc., Waterloo, ON,
Canada) the area bounded between the recovery curve and
O2routine value,
and between the time when the fish exhausted and the time the recovery curve
reached
O2routine
(Fig. 2). Similarly, the cost
of transport through water increases exponentially with swimming speed
(Brett, 1964
;
Webb, 1975
), so it was assumed
that mean
O2
increased exponentially with time during the Ucrit test
because swimming speed was increased in an incremental fashion. The 5 min
steps were adjusted to 20 min steps to ensure a constant relationship between
time and swimming speed throughout the Ucrit test.
|
|
|
Statistical comparisons of EPOC for the first and second swims were compared with a paired Student's t-test. Statistical comparisons among all fish stocks were accomplished using a parametric analysis of variance (ANOVA). In cases where the ANOVA reported significant differences, a pairwise post-hoc Tukey test was used to determine specifically which groups were different.
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Results |
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Using the regression curves, total EPOC was estimated as between 60.9 and
289.8 mg O2 kg-1, depending on the fish stock
(Table 2). The empirical data
from the 45 min recovery period, which ranged from 61.6 to 254.2 mg
O2 kg-1 (Table
2), confirmed the model estimates of total EPOC because the values
agreed to within 2-12%. This close agreement between modeled and measured EPOC
values reflected that fact that
O2 was at or
near
O2routine
following the 45 min recovery period.
|
Modeling the total oxygen cost of swimming to
Ucrit
Regression curves were fitted to the
O2 measurements
made during the Ucrit swim test (solid curves in
Fig. 2A-D). While exponential
curves satisfactorily fitted the data for WVR sockeye salmon and CHE coho
salmon (P<0.05; r2>0.987), a sigmoid
relationship was needed for GC sockeye salmon (P<0.05;
r2>0.995). The area bounded by this curve and
O2routine, and
by the time zero and the end of the Ucrit test,
represented the measured aerobic cost of swimming to Ucrit
(Table 2). The total oxygen
cost of swimming to Ucrit could then be calculated by
adding EPOC to the measured aerobic oxygen, and assuming the non-aerobic
oxygen cost of swimming to Ucrit was equal to EPOC (see
Brett, 1964
). However, because
total oxygen cost of swimming to Ucrit is always relative
to the duration of the Ucrit test, we modeled the total
oxygen cost of swimming by making the further assumption that it would
increase exponentially with swimming speed (and therefore time, as shown by
the broken curves in Fig.
2A-D). The exponential curves that modeled (P<0.05)
the total oxygen cost of swimming to Ucrit were derived by
iterations (r2>0.970) until the total oxygen cost of
swimming to Ucrit matched the measured aerobic oxygen such
that EPOC and the non-aerobic oxygen cost differed by no more than 1.5%
(Table 2). The curve for the
total cost of swimming to Ucrit could then be compared
with the aerobic oxygen cost curve to derive the additional non-aerobic costs
of swimming at a given speed. For example, the non-aerobic costs added an
additional 24.1-50.5% to the
O2max measured
at Ucrit [GC=50.5%, CHE=24.5%, WVR (16°C)=26.0%, WVR
(12°C)=24.1%].
The regression curves for both the total oxygen cost of swimming to
Ucrit and the measured aerobic oxygen cost shared the same
data points below 50% Ucrit, because Burgetz et al.
(1998) suggested that rainbow
trout can reach 70% Ucrit without anaerobic swimming.
These two curves, however, diverged from each other between 55 and 120 min
into the Ucrit test
(Fig. 2), and these times
corresponded to swimming speeds of between 0.86 BL
s1 and 1.30 BL s1, depending on
the salmon stock. This transition to non-aerobic swimming occurred at between
59% and 62% Ucrit. As a result, the non-aerobic cost of
swimming increased the cost of transport (COT:
Fig. 3A) and net cost of
transport (COTnet: Fig.
3B) only at speeds above those associated with minimum cost of
transport.
|
Effect of temperature on EPOC
The longest recovery time was associated with GC sockeye salmon, the salmon
stock tested at the highest ambient water temperature and which reached the
highest Ucrit and
O2max. EPOC
varied exponentially with ambient water temperature
(Fig. 4A) and
Ucrit (Fig.
4B) among the salmon stocks.
|
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Discussion |
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The first caveat is that the shorter recovery time may reflect different
rearing conditions among studies. Both the adult salmon used here and the
Atlantic cod used by Reidy et al.
(1995) were captured from wild
stocks, whereas the earlier work on juvenile salmonids involved
hatchery-raised stocks. Gamperl et al.
(2002
) showed that wild
rainbow trout exhibit a level of aerobic fitness that is at least one-third
greater than hatchery-raised individuals. This heightened aerobic fitness,
presumably related to natural experiences of being exercised, may also favour
a more rapid recovery rate. In addition, the practice swim prior to the
Ucrit test could have lowered EPOC, as seen earlier with
juvenile rainbow trout (Scarabello et al.,
1992
). Scarabello et al.
(1992
) showed that chasing
rainbow trout to exhaustion a second time, after a 6 h recovery period at
15°C, reduced recovery time to 2-3 h and almost halved EPOC to a value
(252 mg O2 kg-1) that was in line with the EPOC for GC
sockeye salmon at 18°C. Farlinger and Beamish
(1977
) similarly found that
practice swims were beneficial for subsequent swimming performance. Adult,
wild salmon may be naturally better aerobic swimmers with or without a
practice swim because
O2max, EPOC and
Ucrit were the same for the first and second
Ucrit.
A second caveat is that the short recovery times may reflect limited
anaerobic swimming in adult, wild fish because they were either less willing
or less able to do so. Our EPOC values, ranging from 55 to 290 mg
O2 kg-1 at temperatures between 8°C and 18°C,
are lower than those either for Ucrit tests with juvenile
(33-63 g) sockeye salmon (252 mg O2 kg-1 at 5°C to
504 mg O2 kg-1 at 15°C;
Brett, 1964) or for chased
juvenile (6 g) rainbow trout (454 mg O2 kg-1 at
15°C; Scarabello et al.,
1992
). We did not establish the level of anaerobic effort by
measuring lactate concentration in either muscle or blood, for a variety of
reasons. Some of the fish had to be returned to the stream to spawn and this
precluded invasive experiments. In any event, opening up the swim tunnel to
obtain a muscle sample would have precluded accurate measurements of
O2 during the
recovery period, and would have jeopardized the second swim. Furthermore,
plasma lactate does not peak until about 1 h after exhaustion, i.e. after EPOC
had subsided, and lactate release from tissue into the blood is suppressed by
moderate swimming during recovery, since plasma lactate increases by only 2-7
mmol l-1 versus 12-25 mmol l-1
(Milligan et al., 2000
;
Farrell et al., 2001a
).
Nevertheless, we have previously swum adult, wild sockeye salmon and found
appreciable increases in plasma lactate concentrations both at
Ucrit and during recovery (3-4 mmol l-1)
(Farrell et al., 1998
), even
with the fish swimming to a lower Ucrit and
O2max than in
the present study. In view of this, we feel that the burst-and-coast swimming
gait observed in the present study when the fish approached
Ucrit reflected a substantial contribution of anaerobic
swimming. In fact, the unusual plateau in the
O2
versus swimming speed curve for GC sockeye salmon can only be
explained by an unusually high anaerobic effort as the fish approached
Ucrit.
It is very unlikely that adult, wild salmon are incapable of high levels of
anaerobic effort when forced to do so. In fact, the opposite is more likely,
because both Pacific and Atlantic adult salmon can become even more severely
exhausted than hatchery-raised rainbow trout, as judged by higher muscle
lactate levels after capture by either angling or commercial fisheries
(Wilkie et al., 1997; Farrell
et al.,
2001a
,b
).
Nevertheless, wild salmon naturally cease feeding and, because these salmon
had stopped feeding up to 3 weeks prior to the experiments, we cannot
eliminate the possibility that dwindling energy stores could have limited
anaerobic effort to some degree. However, while a 5 day starvation period has
been shown to decrease total body glycogen stores and the accumulation of
muscle lactate at exhaustion, it had no effect on EPOC
(Scarabello et al., 1991
).
The third caveat is that we may have underestimated both EPOC and recovery
time because of an elevated
O2routine.
Earlier Brett (1964
) obtained a
`minimum'
O2routine by
omitting any fish exhibiting `restless behaviors'. While we ensured that fish
were undisturbed when
O2routine was
measured, no attempt was made to identify `outliers'. Even so, our
O2routine values
(2.47-4.35 mg O2 min-1 kg-1;
Table 1) were in the range of
previous estimates (1.21-2.92 mg O2 min-1
kg-1; Brett, 1964
;
3.36 mg O2 min-1 kg-1,
Scarabello et al., 1991
), and
so the error due to an elevated
O2routine cannot
be large. Furthermore, if our measurement of
O2routine was
problematic, then a lower EPOC would be associated with a higher
O2routine. This
was not the case for GC sockeye salmon, which had the highest
O2routine as
well as the highest EPOC.
Our data concur with those of Brett
(1964) for juvenile sockeye
salmon, who showed that EPOC and Ucrit were directly
related to water temperature. This conclusion is consistent with the plateau
observed for the
O2 curve for GC
sockeye salmon, which is most likely to be due to a greater anaerobic effort
of white muscle fibres at a higher temperature
(Kieffer et al., 1994
;
Wilkie et al., 1997
). However,
unlike Brett (1964
), we found
that a larger EPOC was associated with a longer recovery time. A longer
recovery rate at warmer temperatures is inconsistent with the faster recovery
rates reported for muscle ATP and glycogen in rainbow trout and Atlantic
salmon (Kieffer et al., 1994
;
Wilkie et al., 1997
).
Electromyography has shown that white muscle fibre recruitment in cyprinids
occurs at 80% Ucrit (e.g.
Rome et al., 1984). In rainbow
trout, accumulation of muscle lactate became a statistically significant
oxygen cost at 80% Ucrit, and though not statistically
significant, the oxygen cost at 70% Ucrit was 24% above
routine (Burgetz et al., 1998
).
We estimated that EPOC began to contribute to the oxygen cost of swimming at
59-62% Ucrit. This lower transition speed compared with
that for an anaerobic swimming gait may be related to disruptions, other than
anaerobic swimming, that contribute to EPOC
(Scarabello et al., 1992
). For
example, the so-called `osmo-respiratory compromise' during exercise
(Randall et al., 1972
;
Nilsson, 1986
), almost doubles
with exercise, with one sodium ion being lost across the gills for every five
molecules of oxygen taken up versus one sodium ion being lost for
every eight molecules of oxygen at rest
(Gonzalez and MacDonald,
1992
). Our modeling, however, does not support the idea that this
type of ionic disruption may add up to 20% to the net oxygen cost of swimming
(Febry and Lutz, 1987
),
because maximally the non-aerobic oxygen cost of swimming added only 24-51% to
O2
(Table 2). By comparison,
Burgetz et al. (1998
) predicted
that anaerobic swimming alone added a 79% oxygen cost at
Ucrit, based on a conversion of whole body lactate to an
oxygen equivalent in hatchery raised rainbow trout. Despite these differences
among studies, it is important to note that the non-aerobic costs of swimming
in adult salmon had apparently very little consequence for the minimum cost of
transport (Fig. 4).
We are unaware of comparable information on adult, wild salmon that would
allow EPOC to be incorporated into an ecologically relevant estimate of the
total oxygen cost of locomotory activity during adult salmon migrations.
Nevertheless, an understanding of the energetic costs of anaerobic swimming is
critical to our understanding of the migration ecology and management of
Pacific salmon. Adult Pacific salmon do not feed during their up-river
migration; they must fuel swimming, maturation of gonads and spawning
behaviours from energy stores, and use bouts of anaerobic swimming
(Hinch et al., 2002). Rand and
Hinch (1998
) developed a
bioenergetics model to predict energy depletion, and the associated risk of
energy exhaustion and premature mortality for up-river migrating Early Stuart
sockeye salmon, to help fisheries managers who make decisions about whether
fisheries should be opened or closed. Their model assumed that anaerobic
swimming was 15% more expensive than aerobic swimming. The present study
clearly shows that this is a significant underestimate (up to three times) of
the true relationship. Anaerobic swimming is thus much more critical to the
energy budgets of sockeye salmon than was previously thought and this fact
must be recognized by fisheries managers who assess the impacts of changing
river flows and temperatures on energy use and hence migration success.
In summary, we have provided the first measurements of EPOC and estimates
of the total cost of swimming to Ucrit among different
stocks of adult, wild salmon. While EPOC varied among fish stocks,
O2routine was
always restored within approximately 1 h. Potential explanations for the
shorter recovery times and lower EPOC values for adult, wild salmon compared
with juvenile, hatchery-reared salmonids are presented. EPOC was estimated to
add 24.1-50.5% to the
O2max measured
at Ucrit, depending on the species, and because this cost
can be three times as high as that used for energetic modeling of salmon
migration up-river, these energetic models may have to be revisited.
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Acknowledgments |
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