On-line venous oxygen tensions in rainbow trout during graded exercise at two acclimation temperatures
Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, V5A 1S6, Canada
* Author for correspondence (e-mail: farrell{at}sfu.ca)
Accepted 23 October 2002
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Summary |
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Key words: venous oxygen tension, exercise, temperature, cold acclimation, warm acclimation, PvO2, heart, swimming speed, rainbow trout, Oncorhynchus mykiss, teleost
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Introduction |
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The venous blood oxygen supply to the fish myocardium apparently becomes
precarious during exercise. For example, in rainbow trout (Oncorhynchus
mykiss), exercise will cause cardiac output to increase by threefold and
ventral aortic pressure to increase by 58%
(Kiceniuk and Jones, 1977),
which in combination will increase the oxygen needs of the heart by over
fourfold (Farrell and Jones,
1992
). While this increased myocardial oxygen demand is met, in
part, by up to a 2.5-fold increase in coronary blood flow to the compact
myocardium during swimming (Axelsson and
Farrell, 1993
; Gamperl et al.,
1995
), the oxygen content in the venous blood decreases
considerably because locomotory muscles extract a greater proportion of oxygen
from the blood to support their increased workload.
This unfavourable change in myocardial oxygen demand compared with oxygen
supply via the cardiac circulation has led to the idea of a threshold
value for the venous partial pressure of oxygen
(PvO2) that would then guarantee an adequate
oxygen supply to the working myocardium
(Davie and Farrell, 1991;
Farrell, 1993
;
Steffensen and Farrell, 1998
).
Davie and Farrell (1991
)
reviewed available data for PvO2 in swimming
fish and suggested that this threshold might be between 6 torr and 16 torr (1
torr=133.3 Pa), i.e. the PvO2 values when fish
quit swimming. Steffensen and Farrell
(1998
) subsequently swam fish
under progressively hypoxic conditions and found that fish quit swimming with
a PvO2 of 7-8 torr. In addition, when the
coronary circulation was ligated to eliminate coronary blood flow to the
compact myocardium, the increase in ventral aortic blood pressure normally
observed during swimming did not occur when
PvO2 had decreased to 13-14 torr. They
concluded that this PvO2 might be the venous
oxygen threshold for adequately supplying the inner spongy myocardium.
Furthermore, Jones (1986
)
suggested that a PvO2 value of 10 torr is
likely to be the absolute limit at which cardiac cells can extract sufficient
oxygen for their needs. However, beyond the theoretical considerations, all of
the data to support the idea of a PvO2
threshold during swimming have involved taking a single venous blood sample
while fish are in the final stages of a critical swimming speed test. We
reasoned that on-line measurement of PvO2 might
provide a much better resolution of whether or not a
PvO2 threshold exists in exercising fish.
A further issue surrounding a PvO2 threshold
concerns the effect of temperature on the venous oxygen reserve. Heath and
Hughes (1973) reported that an
acute increase in temperature produced a decline in the venous blood oxygen
concentration in rainbow trout at a temperature of 24-25°C, and, at these
temperatures, cardiac arrhythmias also developed. One interpretation of these
data is that when temperature is elevated to near the upper lethal limit,
there is a depletion of the venous oxygen reserve in the cardiac circulation,
which results in a catastrophic cardiac hypoxic collapse
(Farrell, 2002
). The
right-shift in the oxygen haemoglobin curve, which is known to occur in fish
blood with temperature acclimation (Perry
and Reid, 1994
), of course would serve to increase the partial
pressure gradient of venous blood reaching the heart, and this could be
advantageous for the myocardial oxygen supply. Consequently, if a venous
oxygen threshold does exist in fish, then the prediction is that the
PvO2 threshold would increase with acclimation
temperature. Thus, the objective of the present study was to measure
PvO2 on line in rainbow trout acclimated to two
acclimation temperatures to provide support for these ideas.
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Materials and methods |
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Experimental protocol
The purpose of the experiments was to monitor
PvO2 in rainbow trout during a graded exercise
challenge. PvO2 was determined using a
fibreoptic micro-optode connected to a Microx 1 oxygen meter from Presens GmbH
(www.presens.de)
chronically implanted into the ductus Cuvier. To implant the optode, fish were
first anaesthetized (0.1 mg l-1 MS222 buffered with 0.1 mg
l-1 NaHCO3) and placed on an operating table, where the
gills were continuously supplied with aerated water containing diluted
anaesthetic (0.05 mg l-1 of MS222 and NaHCO3). The right
operculum and gills were carefully retracted to expose the cleithrum, where a
dorso-ventral incision was made to expose the ductus Cuvier. A small incision
was made in the vein to advance the optode approximately 1 cm retrograde into
the ductus Cuvier. The incision in the vessel was closed around the optode
with a suture (3-0 silk) and minimal blood loss. A second suture was used to
further secure the optode in place. The optode lead was then secured with
sutures placed in the cleithrum, under the right pectoral fin and anterior to
the dorsal fin. The incision in the cleithrum was then sutured and penicillin
was spread on the wound. The gills were irrigated with fresh water until
muscle tone was observed before moving the fish into the swim tunnel. Each
micro-optode was calibrated in oxygen-free water and air-saturated water, as
per manufacturer instructions, and the optode tip was soaked in a 100 IU
ml-1 heparin solution for 5-10 min prior to surgery. The Microx 1
oxygen meter was set to continuously measure % air saturation of oxygen in the
blood, recording a value every 1 s via a serial connection to a
computer.
Fish were allowed to recover for 2 h in a Brett-type respirometer swim
tunnel (as described in Jain et al.,
1997) with a nominal water velocity of 9.6 cm s-1,
which helped orientate the fish while it rested on the bottom of the swim
chamber. The water velocity (cm s-1) in the swim chamber was
calibrated to the frequency readings for the pump before both sets of
experiments using a current meter (Valeport Marine Scientific Ltd., Dartmouth,
UK). A shocking grid, affixed to the rear of the swimming chamber, provided an
electric pulse (3-6 V) to discourage the fish from resting on the rear grid
when the water velocity was increased. Each fish was subjected to two
ramp-critical speed (Ucrit) tests
(Jain et al., 1997
). Our
initial concern was that the optode would not be robust enough to survive
overnight recovery, and therefore the first swim test was performed 2 h after
surgery. However, this concern proved to be unfounded and a second swim test
was possible after a 24-h recovery period post-surgery. Both swim tests used
the same protocol. The ramp phase of the swim test consisted of seven
increments of 5 cm s-1 every 5 min to bring to the fish to
approximately 50% of the anticipated Ucrit value.
Subsequently, each velocity increment of 5 cm s-1 lasted 15 min or
until the fish fatigued, as indicated by either the tail or the entire fish
impinging on the rear shocking grid for 10 s. During each test, unsteady
swimming was usually noted, categorized as either `burst-and-coast swimming'
or `fighting', and related to the PvO2.
Burst-and-coast swimming consisted of an increase in swimming speed with
directed forward motion, usually from the back to either the middle or the
front of the working section of the tunnel. A fight was classified as more
erratic and longer movement, often lacking direct forward motion.
PvO2 was recorded continuously every 1 s during
the 2-h recovery period post-surgery, immediately prior to and during both
swim tests, and during a 2-h recovery period following each of the swim tests.
After the recovery period of the second swim test, the fish was re-fatigued
using a high water velocity, removed from the swim tunnel and reanaesthetized
(0.1 mg l-1 MS222 and NaHCO3). The optode was removed
and the wound sutured, after which the fish was revived with fresh water and
returned to the outdoor tank.
Data analysis
Values of PvO2 were recorded as % air
saturation. Using equations and a spreadsheet provided by Presens GmbH, these
values were adjusted for minor temperature differences and for ambient
atmospheric pressure. These values were then converted to
PvO2 (torr; 1 torr=133.3 Pa) using the
following equation:
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Mean PvO2 for each step was determined by
averaging the PvO2 values from steady-state
swimming during the final 25% of each velocity increment. This task was made
easier because it turned out that unsteady swimming behaviours were typically
associated with unsteady PvO2 values (see
below). PvO2 values during unsteady swimming
were omitted from the calculation of mean values and were dealt with
separately by reporting the minimum PvO2 due to
a burst-and-coast swimming or fighting behaviour. Ucrit
(cm s-1) was calculated using the equation:
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Water velocities were adjusted for the solid blocking effect
(Bell and Terhune, 1970) using
the length (l), width (w) and area (A) of the fish.
The fractional uncorrected swimming speed
(FS)=0.5(l/w), and the proportional error due to
solid blocking
(ES)=(0.8FS)(A/324.3)1.5.
All water velocities values were multiplied by (1+ES),
standardized to body length s-1 for comparisons and presentation,
and presented as means ± S.E.M. for each swim. Statistical comparison
of Ucrit values was performed using a one-way analysis of
variance (ANOVA). For comparisons between groups, mean incremental velocities
were determined and presented as a percentage of the
Ucrit. PvO2 values for
similar %Ucrit values were pooled and averaged. All water
velocities, %Ucrit and PvO2
values are presented as means ± S.E.M. Statistical comparisons between
the control and Ucrit values for the first and second swim
tests were performed using a paired t-test (Sigma Stat 2.0). The
comparisons within a graded swim test were performed using a repeated-measures
ANOVA. For this comparison, measurements between 11% and 39%
Ucrit and 10% and 29% Ucrit for cold-
and warm-acclimated fish, respectively, were excluded because many of the fish
did not show steady-state swimming. Also, in each acclimation group, one fish
was removed from the comparison because of missing steady-state data, making
repeated measures impossible. A Student's t-test was used for
comparisons between acclimation temperatures. Statistical significance was
assigned when P<0.05. For the three recovery periods, a recovery
curve for PvO2 was generated by pooling values
for each fish at common times. For the warm-acclimated fish, the recovery
curves represent values (means ± S.E.M.) taken at 1 s intervals for the
entire 2-h recovery period. Similar data are presented for cold-acclimated
fish, with the exception that the data were recorded only every minute for the
final 30 min of the recovery from the initial swim.
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Results |
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Ucrit for warm-acclimated fish (1.98±0.19 body lengths s-1 and 2.05±0.17 body lengths s-1 for first and second swim tests, respectively) was significantly higher than that for cold-acclimated fish (1.32±0.07 body lengths s-1 and 1.47±0.08 body lengths s-1 for first and second swim tests, respectively). Therefore, to facilitate comparisons of steady-state PvO2 values, swimming velocities were expressed as a percentage of the respective Ucrit value (Fig. 2). It was clear from the mean values, as well as individual recordings and visual observations, that swimming performance and PvO2 during the first swim test (inset Fig. 2) were more erratic compared with the second swim test because of a greater proportion of burst-and-coast-type swimming behaviours. Consequently, the first test was regarded as a habituation swim and the comparisons made below relate only to the results for the second swim test.
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Steady-state swimming
For both cold- and warm-acclimated fish,
PvO2 decreased significantly with increasing
swimming speed (Fig. 2). The
decrease in PvO2 was statistically significant
at 69% Ucrit for the cold-acclimated fish but not until
100% Ucrit for the warm-acclimated fish
(Fig. 2). In addition,
PvO2 tended to be higher for warm-acclimated
fish throughout the swim test, although statistical significance was reached
only at velocities of 49% Ucrit. This situation came
about because PvO2 tended to decrease at a
lower %Ucrit for cold-acclimated fish than for
warm-acclimated fish. Importantly, warm-acclimated fish quit swimming at a
significantly higher PvO2 than did
cold-acclimated fish (Fig. 2)
despite the fact that they were swimming at a higher velocity.
The examples of on-line PvO2 recordings for individual fish (Fig. 3) illustrate several important points. Foremost, as fish approached Ucrit, there was a minimum value for PvO2. In fact, PvO2 reached a plateau for both swims with cold-acclimated fish (Fig. 3A,B; see also Fig. 2) and for the first swim with warm-acclimated fish (Fig. 3C; see also inset in Fig. 2). Second, the more erratic nature of the first swim compared with the second swim can be seen clearly by comparing Fig. 3A with Fig. 3B. Finally, the individual PVO2 recordings reflected the cessation of swimming behaviour as fish approached fatigue, i.e. the fish resting on the rear grid. This resting behaviour caused a modest but progressive increase in PVO2 just prior to the termination of the test (Fig. 3A-C).
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Unsteady swimming
Burst-and-coast swimming and, in particular, fighting behaviours produced
characteristically abrupt decreases in PVO2 of varying
magnitude (Fig. 3). Such
behaviours often occurred whenever there was an incremental increase in the
water velocity. While Fig. 3A
shows the most extreme effect on PVO2 that was observed
for either swimming behaviour, overall the associated decrease in
PVO2 rarely went below the minimum
PVO2 observed at Ucrit. This point is
illustrated in Fig. 4, where
minimum PVO2 values associated with unsteady swimming are
presented as a percentage of the minimum PVO2 at
Ucrit. Of the 37 instances that PVO2
decreased to within 60% of the minimum PVO2 at
Ucrit, there were only two instances where
PVO2 decreased to more than 10% below the minimum
PVO2 at Ucrit
(Fig. 4B). Both instances were
for cold-acclimated fish and neither occurred when fish were swimming at a
velocity greater than 80% Ucrit. A similar pattern was
seen for the first swim (Fig.
4A), despite the more erratic swimming behaviours. Collectively,
these data lead us to conclude that the minimum PVO2
values that were recorded near or at Ucrit are threshold
PVO2 values.
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Discussion |
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Measurement of PVO2 in the ventral aorta is easier than
in veins because fish veins typically collapse when blood is withdrawn
(Capra and Satchell, 1977).
Nevertheless, there is very good agreement between the control
PVO2 measured in the ductus Cuvier of resting fish in the
present study (36.9 torr and 47.6 torr;
Fig. 2) and several ventral
aortic PVO2 measurements made previously with rainbow
trout (44 torr, Kiceniuk and Jones,
1977
; 31 torr, Eddy et al.,
1977
; 36 torr, Steffensen and
Farrell, 1998
). The exception is a pre-exercise ventral aortic
PVO2 of 19 torr reported by Stevens and Randall
(1967
). Based on the above
comparisons with previous studies, we are confident that the optode system
provided reliable on-line measurements of PVO2 in rainbow
trout during graded exercise and that reliable conclusions can be drawn
concerning the idea of a PVO2 threshold.
The minimum PVO2 values at Ucrit
were 15.3 torr for cold-acclimated fish and 28.9 torr for warm-acclimated
fish. Similar to the present study, Kiceniuk and Jones
(1977) reported that
PVO2 decreased to 21 torr at Ucrit for
normoxic rainbow trout performing a Ucrit test at
11°C. (However, it is not explicitly stated whether the measurement was
made with blood sampled from the cardinal vein or the ventral aorta.) By
contrast, Stevens and Randall
(1967
) observed no appreciable
change in the pre-exercise PVO2 (19 torr) when rainbow
trout were exercised for 15 min at 4-8°C. Environmental hypoxia can also
lower PVO2. For example, PVO2
decreased to 5 torr with hypoxia (water oxygen tension, 30 torr;
Thomas et al., 1994
).
Similarly, rainbow trout quit swimming (at approximately 70%
Ucrit) when progressive hypoxia had reduced
PVO2 to 7 torr
(Steffensen and Farrell,
1998
).
While the above comparisons are important to make, a cautionary note is
that, at a given level of tissue oxygen demand and arterial blood saturation,
PVO2 is determined in part by cardiac output and blood
haemoglobin concentration, as well as the oxygen saturation level. Therefore,
until this additional information is available, comparison of
PVO2 values must remain rather superficial. This is
particularly the case when different protocols are used. For example, when
rainbow trout were swum at a constant speed and made progressively hypoxic
until they quit swimming (Steffensen and
Farrell, 1998), cardiac performance was probably not as high as in
the present experiments where the fish were swum to Ucrit
under normoxic conditions. With a lower cardiac work and myocardial oxygen
demand, the PvO2 at which the heart can no
longer maintain maximum performance is expected to be lower. Such
considerations help explain why Davie and Farrell
(1991
) suggested a rather large
range for threshold PvO2 of 6-16 torr when all
available data were considered, while Steffensen and Farrell
(1998
) suggested a narrower
threshold PvO2 of 8.6-11.1 torr for hypoxic
rainbow trout acclimated to 15°C and swimming at 70%
Ucrit. The present study suggests that for normoxic
rainbow trout swum to Ucrit at 6-10°C, the threshold
PvO2 was 15 torr
(Fig. 2).
The PvO2 plateau of 15 torr for
cold-acclimated fish suggests to us that swimming at velocities in excess of
approximately 85% Ucrit involved a recruitment of only
white glycolytic fibres. [The present data cannot eliminate the possibility of
cardiac output being increased further, but Gallaugher et al.
(2001) showed that adjustments
to cardiac output were very small in Chinook salmon (Oncorhynchus
tschawytscha) at swimming velocities greater than 80%
Ucrit.] Consistent with this suggestion are the findings
of Burgetz et al. (1998
), who
showed that anaerobic metabolism is required to support swimming speeds
greater than 70% Ucrit in rainbow trout. At 70%
Ucrit and 80% Ucrit, anaerobic
metabolism was estimated to contribute approximately 25% of the oxygen
consumption, and this value increased to 77% at 100%
Ucrit. Rome et al.
(1985
) used electromyogram
recordings to show that the initial recruitment of white muscle in carp
occurred at lower velocities in cold-acclimated fish compared with
warm-acclimated fish. The present results appear to be consistent with this
finding because the plateau for PvO2 occurred
much closer to 100% Ucrit in warm-acclimated compared with
cold-acclimated rainbow trout. However, we do not know if the initial
recruitment of white muscle is aerobic and whether or not white muscle is
capable of a greater range of aerobic performance at warmer temperatures. In
fact, Taylor et al. (1997
),
who measured regional blood flow in exercising rainbow trout, reported that
blood flow to white muscle was significantly higher in 18°C-acclimated
fish compared with 11°C-acclimated fish.
A new idea that is now explored is the possibility that the switch from red
oxidative muscle fibres to glycolytic muscle fibres during high-speed swimming
in rainbow trout is not only orderly but also serves to preserve a reserve of
oxygen in the venous blood. The underlying mechanisms that could bring this
about are a matter for speculation. However, two possibilities are worth
exploring. First, a diffusion limitation for oxygen exchange at the skeletal
muscle may develop as fish swim faster and this would then set an upper limit
for oxygen extraction in locomotory tissues. This could occur because either
the transit time through capillaries in red muscle becomes too short as red
muscle perfusion increases with increasing cardiac output or (and probably in
addition to) white glycolytic muscle fibres have a lower capillary density
(Taylor et al., 1997), which
creates longer diffusion distances. Thus, the anatomical arrangement of
capillaries in fish skeletal muscle probably represents a perfusion-limited
system for oxygen under routine conditions, but one that approaches or becomes
diffusion-limited as fish exercise at levels near to their
Ucrit. This diffusion limitation for oxygen may be such
that sufficient oxygen remains in venous blood to supply the heart adequately.
The other possibility would involve oxygen receptors on the venous side of the
circulation that could, through central integration, produce an efferent
neural output to constrict muscle arterioles and thereby limit muscle blood
flow when PvO2 is near the threshold.
Rather than invoking some anatomical design feature or physiological
regulatory mechanism to explain the venous oxygen reserve, a simple
alternative is that the portion of cardiac output that perfuses non-locomotory
tissues provides the venous oxygen reserve. Limited data on the regional
distribution of blood flow in rainbow trout allow us to explore this
alternative possibility, although the outcome seems to be that oxygen
extraction by skeletal muscle is far from complete. Randall and Daxboeck
(1982) reported that in
resting rainbow trout approximately 52% of blood flow was directed to
locomotory muscles (8.9% to red lateral muscle; 37.4% to white muscle; 5.2% to
pink muscle) and 48% to the rest of the body. At 80%
Ucrit, when cardiac output had tripled, approximately 69%
of the blood flow was now directed to locomotory muscles (42% to red lateral
muscle; 1.1% to white muscle; 25.5% to pink muscle) and 31% to the rest of the
body. If we assume that oxygen supply in the venous circulation returning from
the rest of the body at Ucrit was the same as that
measured in the ductus Cuvier of resting fish, i.e. there was no net change in
oxygen extraction in non-locomotory tissues, then this 31% of cardiac output
would return 3.3 ml O2 s-1 to the heart (i.e. 30% of 11
ml O2 s-1; see below and
Fig. 5). Because this amount is
less than the 5 ml O2 s-1 that we estimate was returning
to the heart during exercise (Fig.
5), blood leaving the locomotory muscles must make up the
difference of 1.7 ml O2 s-1. This would mean that the
venous oxygen content of blood leaving locomotory muscles during exercise
would be approximately 73% lower than that in the resting fish. Nevertheless,
these theoretical calculations, which suggest that only one-third of the
venous oxygen reserve comes from blood leaving locomotory muscle, probably
underestimate this contribution based on the following concern.
|
The blood flow distributions used in the above analysis were based on a
microsphere injection methodology, but it has been suggested that this is an
unreliable methodology for estimating splanchnic blood flow in fish
(Farrell et al., 2001). When
gut blood flow was simultaneously measured with an ultrasonic flow probe and
with microspheres, there was very poor agreement between the two methodologies
under a variety of conditions (Crocker et
al., 2000
). Two additional findings suggest that perhaps the
entire blood flow distribution pattern as revealed by the microsphere
methodology should be treated with caution, and, if anything, the estimate
that non-locomotory tissues receive 31% of cardiac output in exercising
rainbow trout (which is actually an increase in total blood flow from 6.2 ml
min-1 kg-1 to 11.8 ml min-1 kg-1;
Randall and Daxboeck, 1982
) is
too high. First, Neumann et al.
(1983
) used the microsphere
method to estimate that 30% of cardiac output in rainbow trout went to red
muscle and 68.2% went to white muscle 5 min after exhaustive activity. Thus,
with <2% of cardiac output going to non-locomotory tissues, a 10-fold
discrepancy exists between the two studies in the estimates of non-locomotory
tissue blood flow. Second, Thorarensen et al.
(1993
) measured a 60% decrease
in gut blood flow in exercising Chinook salmon at Ucrit
using Doppler flow probes. Consequently, given a decrease in gut blood flow
with exercise and the fact that gut blood flow normally represents 30% of
cardiac output (Thorarensen et al.,
1993
), it seems unlikely that non-locomotory muscle would only
decrease from 48% to 31% of cardiac output. Why more blood flow was not
diverted to locomotory muscles will remain a mystery until further studies on
blood flow distribution and its control are performed on fish. For the present
purpose, it is suffice to say that a protected venous oxygen reserve does
exist when rainbow trout approach Ucrit and, minimally,
one-third of this oxygen reserve has escaped being used by the locomotory
muscles, although these muscles were using glycolysis to power
contractions.
Although we can only speculate on a mechanism to explain the venous oxygen reserve, it is important to note that the effect of unsteady swimming behaviours on PvO2 provided further support for a protected venous oxygen reserve at high swimming speeds. PvO2 would decrease dramatically with unsteady swimming behaviours that are known to recruit white muscle fibres, but rarely did these swimming behaviours decrease PvO2 below the threshold level (Fig. 4). Furthermore, once the fish had reached the threshold PvO2, burst-and-coast swimming seemed to have little impact on PvO2. In fact, whenever the fish rested temporarily on the rear screen of the swim chamber, PvO2 tended to increase, presumably because oxygen extraction by the muscle decreased.
As predicted, the minimum PvO2 was higher for the warm-acclimated fish and this reflected a general increase in PvO2 for the warm-acclimated fish, although statistical significance was reached only at swimming velocities greater than 50% Ucrit. In contrast to the cold-acclimated fish, however, a plateau in PvO2 was not maintained over a substantial range of the higher swimming velocities, except during the habituation swim when the final PvO2 was slightly lower than the second swim (i.e. 23.8 torr versus 28.9 torr) but still higher than the minimum PvO2 for cold-acclimated fish. Thus, it is possible that warm-acclimated fish only approached, and did not quite reach, a threshold PvO2.
The higher minimum PvO2 for warm-acclimated
compared with cold-acclimated fish may translate to an improved cardiac oxygen
supply for the warm-acclimated fish, because rates of oxygen diffusion could
be faster (due to a larger partial pressure gradient). This could help support
the faster rate of cardiac contraction and the higher level of cardiac work
also associated with elevated temperature
(Aho and Vornanen, 1999).
However, this benefit might be negated if venous oxygen content was not
preserved. As neither venous oxygen content nor oxygen dissociation curves
were measured in the present study, we have used literature values to generate
theoretical curves for venous oxygen delivery to the heart at the two
acclimation temperatures (Fig.
5). An oxygenhaemoglobin dissociation curve for venous
blood was taken from Thomas et al.
(1994
) for 10°C rainbow
trout. A Bohr coefficient was used to adjust an oxygenhemoglobin
dissociation curve for arterial blood at 15°C (taken from
Perry and Reid, 1994
) and
generate a venous curve for the warm-acclimated fish. The haemoglobin
concentration was assumed to be such that fully saturated blood contained 10
vols% oxygen (Gallaugher et al.,
1995
), routine cardiac output was assumed to be 17 ml
min-1 kg-1 for cold-acclimated fish
(Kiceniuk and Jones, 1977
) and
25 ml min-1 kg-1 for warm-acclimated fish, and a 1 kg
fish was assumed to have a 1 g ventricle
(Farrell et al., 1988
). These
assumptions allowed venous oxygen delivery to the heart (ml O2
s-1 g ventricle mass-1) to be calculated from the
product of cardiac output (ml O2 s-1 g ventricle
mass-1) and venous oxygen concentration (mg O2
ml-1; calculated from % haemoglobin saturation at a given partial
pressure). The results show that at the PvO2
values measured in resting fish (36.9 torr and 47.6 torr for cold- and
warm-acclimated fish, respectively), the venous oxygen delivery to the heart
was quite similar despite the differences in
PvO2 (11.0 ml O2 s-1 g
ventricle mass-1 and 13.5 ml O2 s-1 g
ventricle mass-1, respectively). The
PvO2 at 100% Ucrit
(15.3 torr and 28.9 torr for cold- and warm-acclimated fish, respectively)
obviously reduced venous oxygen content, but a 2.1-fold increase in cardiac
output would have been adequate to maintain venous oxygen delivery to the
heart at the level estimated for resting fish (see open symbols in
Fig. 5). As cardiac output can
increase by 2.5-fold to 3.0-fold at Ucrit
(Kiceniuk and Jones, 1977
;
Thorarensen et al., 1996
),
these theoretical estimates lead to the conclusion that venous blood oxygen
delivery via the cardiac circulation is similar in warm-acclimated
and cold-acclimated rainbow trout whether they are resting or swimming at 100%
Ucrit. However, for exercising fish, the oxygen partial
pressure gradient driving oxygen diffusion to the myocardium decreases
approximately 2-fold, while myocardial oxygen demand increases approximately
4-fold. In addition, any increase in heart rate associated with exercise will
mean that the residence time of blood in the lumen of heart decreases
proportionately. These changes suggest that, in exercising fish, the rate of
oxygen diffusion to the myocardium is likely to be far more precarious than
the rate of oxygen supply by the cardiac circulation. This then argues for the
need of a PvO2 threshold to ensure an adequate
rate of oxygen diffusion from the cardiac circulation to support the
myocardial oxygen demand during exercise and prevent hypoxic cardiac collapse
near Ucrit.
The right-shift in oxygenhaemoglobin dissociation curve with increasing temperature in fish is generally regarded as favouring oxygen unloading at the locomotory muscles but being unfavourable for oxygen extraction from water when it contains less oxygen than does colder water. However, what has not been considered previously is that the right-shift also favours oxygen delivery to the myocardial tissues via the cardiac circulation. In the present experiments, there was almost a doubling of this gradient at 100% Ucrit for warm-acclimated fish. As an increase in temperature also increases the rate of diffusion of gases, and this cannot be avoided, perhaps the right-shift in the oxygenhaemoglobin dissociation curve co-evolved as a mechanism to also protect the oxygen supply to the heart via the cardiac circulation. While allowing unloading of oxygen from blood to muscles to increase in association with the higher workloads that are possible at warmer temperatures, the right-shift also resulted in an elevated partial pressure gradient for oxygen to cardiac tissues without compromising the overall venous oxygen delivery rate to the heart.
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