The effects of sustained exercise and hypoxia upon oxygen tensions in the red muscle of rainbow trout
1 School of Biosciences, University of Birmingham, Birmingham B15 2TT,
UK
2 Department of Biological Sciences, Simon Fraser University, 8888
University Drive, Burnaby, BC, V5A 1S6, Canada
3 Department of Biology and Chemistry, City University of Hong Kong, Tat
Chee Avenue, Kowloon, Hong Kong, China
4 Department of Physiology, University of Birmingham, Birmingham
B15 2TT, UK
* Author for correspondence at present address: CNRS/IFREMER, CREMA L'Houmeau, BP 5, 17137 L'Houmeau, France (e-mail: David.Mckenzie{at}ifremer.fr)
Accepted 20 July 2004
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Summary |
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Key words: O2-sensitive optode, Root effect, O2 partial pressure, arterial blood O2 content, O2 consumption, swimming
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Introduction |
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Measurements of O2 tensions in the skeletal musculature of
teleost fish would be particularly informative for two other reasons. One of
these is to investigate the extent to which convective O2 supply
might be a limiting factor in the performance of sustained aerobic exercise.
During sustained exercise in tetrapods, increased muscle O2 demand
relative to rates of supply causes a reduction in muscle
PO2 (Jung
et al., 1999; Behnke et al.,
2001
), and fatigue is associated with a severe decline in
intramuscular O2 tension
(Molé et al., 1999
;
Howlett and Hogan, 2001
). Fish
support sustained swimming activity with their RM, while WM powers the faster,
unsteady sprint and burst swimming activities
(Bone, 1978
). Therefore,
measurements of PRMO2 during
swimming would provide insight into whether RM O2 supply is a
factor limiting the performance of sustained swimming, that is, whether
exhaustion is associated with a profound decline in
PRMO2.
Another reason why PRMO2 of
teleosts might be particularly interesting relates to a unique characteristic
of some teleost haemoglobins, the Root effect
(Root, 1931). When blood pH
drops, haemoglobins with a Root effect exhibit a markedly reduced capacity to
bind O2, and hence will release bound O2
(Root, 1931
;
Randall, 1998
;
Pelster and Randall, 1998
). A
well established physiological role for the Root effect is found in
specialised vascular beds (retes), where high rates of lactic acid and
CO2 production by specialised cells generate low pH, resulting in
localised PO2 values that are considerably
higher than in arterial blood leaving the gills, due to unloading of
O2 from haemoglobin. In particular, the choroid rete ensures that
photoreceptors in the retina are well oxygenated, while the rete mirabilis
provides O2 to inflate the swimbladder and maintain buoyancy as
fish descend in the water column (Jensen
et al., 1998
; Pelster and
Randall, 1998
).
Theoretically, the Root effect may also promote the release of
O2 from haemoglobin at other respiring tissues. This is because
in vitro evidence shows that diffusion of respiratory CO2
into the teleost erythrocyte, and its carbonic anhydrase-catalysed hydration
to HCO3 and H+, occurs more rapidly
than diffusional release of O2 from haemoglobin in response to a
PO2 gradient
(Brauner and Randall, 1998;
Pelster and Randall, 1998
).
Consequently, a transient drop in erythrocyte pH following the catalysed
hydration of CO2 could elicit a Root effect and generate high
PO2 values in well-vascularised aerobic
tissues. The presence and extent of this effect in tissues other than retes,
such as RM, has not been studied. If measurements of
PRMO2 revealed that it was higher
than the PO2 of arterial blood leaving the
gills (PaO2), then this would be dramatic
evidence that the Root effect influences O2 tensions in aerobic
tissues.
In the current study, novel O2-sensitive optical fibre sensors
(`micro-optodes') were used to measure the
PRMO2 of conscious free-swimming
rainbow trout, a species with a pronounced Root effect
(Binotti et al., 1971).
Measurements were made under three regimes: during normoxia, to compare with
data reported for mammalian skeletal muscles
(Hutter et al., 1999
;
Jung et al., 1999
;
Suttner et al., 2002
;
Behnke et al., 2001
) and to
investigate whether the Root effect contributes to elevated
PRMO2; during graded sustained
exercise, to gain insights into RM O2 supply during an increase in
demand, and also during mild hypoxia, to investigate whether reducing the
arterial-to-tissue PO2 gradient would expose an
impact of the Root effect upon
PRMO2.
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Materials and methods |
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Surgical preparation and measurement of red muscle PO2
Fish were anaesthetised in 0.1 mg l1 MS-222 buffered with
0.1 mg l1 NaHCO3, and then transferred to an
operating table where their gills were irrigated with aerated water containing
diluted anaesthetic (0.05 mg l1 MS-222 and
NaHCO3). A small incision was made in the skin just dorsal to the
lateral line to reveal the underlying RM sheet. A blunted surgical needle (15G
Terumo, Leuven, Belgium) was then advanced under the skin for approximately 1
cm, with the foremost end of the blunted needle bevel against the underside of
the skin. Great care was taken to avoid penetrating the underlying
musculature. An oxygen-sensitive optical chemical fibre sensor (PreSens;
Precision Sensing GmbH, Regensburg, Germany), with a tapered Teflon-coated tip
(diameter <10 µm), was inserted into the bore of the needle and advanced
until the tip reached the end of the needle. The needle was then angled at
approximately 45° to the skin such that the bevelled end rested flat
against the musculature and the tip of the optode advanced gently, at the
prevailing angle of 45°, for approximately 3 mm into the underlying sheet
of RM. The needle was then withdrawn along the optode lead, and the optode
secured in position with sutures to the skin. Trout were then cannulated in
the dorsal aorta (DA) using the technique described by Soivio et al.
(1975).
While the trout were still under anaesthesia, the optode was connected to a
Microx 1 oxygen meter (PreSens), connected in turn via a serial port
to a PC with dedicated software, which displayed
PRMO2 at the optode tip every 1 s
and saved a measure of PRMO2 every 1
min in an ASCII file. Prior to surgery, each optode was calibrated in
oxygen-free and air-saturated water, and the tip soaked for 10 min in 100 i.u.
ml1 heparin (Farrell and
Clutterham, 2003). The position of the probe in the RM was
confirmed post-mortem by careful dissection under a binocular
microscope. Data are reported only for those experiments where the probe could
be recalibrated, post-mortem, to correct for any drift, according to
the manufacturer's instructions. In one case where blood clotting and tissue
damage were visible around the tip of the probe, the results were
disregarded.
Fish were recovered for approximately 42 h in normoxic water while swimming
gently at a speed equivalent to 0.5 body lengths s1
(BL s1) in the Brett-type swimming respirometer
described in Gallaugher et al.
(1995), and
PRMO2 was measured every 1 min
throughout. The DA cannula was flushed every 24 h with heparinised (10 i.u.
ml1) teleost saline. Measurements of control normoxic
PRMO2 values were made while the
animals were swimming gently so as to establish a constant level of muscular
work and consequent O2 demand and to reduce spontaneous changes in
activity level, thus minimising variability in
PRMO2 (see
Fig. 1).
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Sustained exercise
Exercise performance was measured by exposing the fish to 0.5 BL
s1 increments in swimming speed every 30 min until fatigue.
Maximum sustainable swimming speed (Ucrit) was calculated
as described by Brett (1964).
The PRMO2 was measured every 1 min
throughout, while PaO2, arterial blood total
O2 content (CaO2) and arterial blood
pH (pHa) were measured once at each swimming speed, at fatigue, and at 1 h and
2 h post-fatigue. The PaO2 was measured by
gently withdrawing blood along the DA catheter and into a glass cuvette (D616,
Radiometer, Copenhagen, Denmark) containing an oxygen electrode (Radiometer
E5046), thermostatted to the experimental temperature, with the signal
displayed on a Radiometer PHM72 acidbase analyser. A subsample of this
arterial blood was withdrawn (300 µl) and
CaO2 measured as described by Tucker
(1967
) using a Radiometer
O2 electrode thermostatted to 37°C, and pHa measured using a
Radiometer BMS2 capillary pH electrode thermostatted to the same water
temperature as the fish, with the signals displayed on a Radiometer PHM73
acidbase analyser. The remaining blood, plus 300 µl of saline, was
returned to the animal. Water PO2
(PwO2) was monitored continually using an
oxygen-sensitive galvanic cell and associated meter (HO1G, Oxyguard,
Birkerød, Denmark) with the signal displayed on a chart-recorder. The
PwO2 recording was used to measure oxygen
consumption by the fish
(
O2, in mg
kg1 h1) in the sealed respirometer over 20
min at each swimming speed, then for a 30 min period centred around 1 h and 2
h recovery, using the techniques described in Gallaugher et al.
(1995
). For the analysis of
the effects of exercise, mean values were derived for the measured variables
under control conditions (i.e. exercising gently at 0.5 BL
s1); for fish swimming at a common degree of sustained
exercise (1 BL s1); for the maximum speed which the
fish were able to sustain for a complete 30 min measurement interval (this
ranged from 1 to 1.5 BL s1); immediately at
exhaustion; and then at 1 h and 2 h of recovery. An indication of changes in
blood O2 supply during aerobic exercise was obtained by resolving
the Fick equation:
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Exposure to hypoxia
While swimming gently at a speed of 0.5 BL s1,
the trout were exposed to two levels of mild hypoxia, comprising 30 min at 100
mmHg, followed by 30 min at 75 mmHg, followed by 1 h recovery to normoxia (140
mmHg). The PRMO2 was monitored every
1 min throughout the exposure protocol. Water
PO2 was monitored continually, and water
entering the respirometer made hypoxic by passing it counter-current to a flow
of compressed 100% N2 in a gas-exchange column. The
PwO2 recording was used to measure
O2 in the sealed
respirometer for 30 min in normoxia, for 30 min at both levels of hypoxia, and
for 30 min centred upon 1 h recovery to normoxia. A measurement of
PaO2 was made every 5 min by gently withdrawing
blood along the DA catheter and into the O2 electrode cuvette.
Samples of arterial blood (300 µl, replaced immediately with an equal
volume of saline) were collected from the DA cannula in normoxia, at 30
minexposure to each level of hypoxia, and following 1 h recovery to normoxia,
to measure CaO2 and pHa.
The HbO2 dissociation curve derived for rainbow trout at
14°C by Farrell and Clutterham
(2003) was used to identify
the percentage haemoglobin saturations that would prevail in blood at the
PO2 measured in the dorsal aorta and in the RM,
in normoxia and at each level of hypoxia. The total O2 content of
blood in the RM (CRMO2, in mmol
ml1) was then estimated as follows:
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Data analysis and statistics
One-way analysis of variance (ANOVA) for repeated measures was used to
reveal effects of exercise or hypoxia on any single variable. A two-way
repeated-measures ANOVA was used to assess the effects of progressive hypoxia
on PaO2 versus
PRMO2. Where changes in
PO2 were expressed as a percentage of the
normoxic value, data were arc-sine transformed prior to analysis by ANOVA. In
all cases, Bonferroni post-hoc tests were used to identify where
significant differences lay. A probability of less than 5%
(P<0.05) was taken as the fiducial level for statistical
significance.
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Results |
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Effects of sustained exercise
As expected, exercise caused an exponential increase in O2
uptake, and the maximum rate of
O2 was observed
at the maximum speed which the fish were able to sustain for a complete 30 min
interval (Fig. 2). Exercise
also caused a decline in pHa, particularly at Ucrit
(Fig. 2), which is evidence of
a switch to glycolytic metabolism prior to exhaustion. Nevertheless, trout in
the current study did not exercise exceptionally well, reaching a
Ucrit of 1.38±0.16 BL s1
(N=5), which is lower than the Ucrit of
approximately 2.0 BL s1 reported earlier for
chronically instrumented rainbow trout at the same temperature (e.g.
Shingles et al., 2001
;
Farrell and Clutterham, 2003
).
Arterial blood PO2 also showed a significant
reduction during sustained exercise and at exhaustion, but recovered rapidly,
unlike both
O2
and pHa, which slowly returned towards control values during 2 h of recovery.
Despite the arterial acidosis, CaO2 was
unchanged throughout exercise and at exhaustion
(Fig. 2).
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During sustained exercise, PRMO2
showed a significant drop and although the mean value remained above 40 mmHg,
PRMO2 never exceeded
PaO2. Moreover,
PRMO2 rose significantly at the
moment of exhaustion to a level that was not statistically different from the
control, and remained thus for the ensuing 2 h recovery period. The partial
pressure gradient between arterial blood and the RM dropped as exercise
intensity increased, to a low at fatigue, but then returned rapidly to control
values during recovery (Fig.
2). Given that the partial pressure gradient dropped as
O2 increased
during exercise, resolution of the Fick equation revealed that O2
delivery, hence blood flow, to the red muscle would have to increase by a
factor of 4.6±1.1 times (mean ±
S.E.M., N=5) between swimming speeds
of 0.5 BL s1 and 1.38 BL
s1.
Effects of exposure to hypoxia
Mild hypoxia had no significant effects on
O2 and
CaO2 (Table
2), so it could be assumed that rates of tissue O2
demand and blood O2 transport capacity did not change
significantly. Furthermore, the absence of any changes in pHa indicates that
there was no major increase in the release of lactic acid and CO2
from the tissues (Table 2).
Thus, the most significant effect of mild hypoxia was a decrease in the
PO2 of arterial blood as it left the gills
(Table 1). Correspondingly, the
PRMO2 showed close temporal
sensitivity to changes in PwO2 and
PaO2 during exposure to hypoxia and the return
to normoxia (Fig. 3). Red
muscle PO2 was significantly reduced from
normoxic values at both levels of hypoxia
(PwO2=100 mmHg and 75 mmHg), but changes in
PRMO2 were significantly less than
those in PaO2, and so the arterial to RM
PO2 gradient declined as hypoxia deepened
(Fig. 3,
Table 1). Proportional (%)
changes in PO2, relative to normoxic values,
were much more pronounced than the net changes in the RM but, nonetheless,
were significantly smaller in the RM than in the arterial blood
(Fig. 3, Table 1). At no time during
either hypoxia or recovery did any fish exhibit a higher
PRMO2 than their
PaO2. In fact, the estimates of apparent
O2 unloading did not decrease as hypoxia deepened but, rather,
increased slightly (Table
2).
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Discussion |
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Farrell and Clutterham
(2003) also found that
PvO2 dropped precipitously to around 20 mmHg
whenever the fish struggled, and attributed this to sudden increases in muscle
O2 extraction. The sharp reductions in
PRMO2 that were observed when fish
struggled could be due either to increased O2 demand and
extraction, or to a decrease in local blood flow associated with struggling
behaviours. The latter may be the main contributing factor, as struggling
behaviours are associated with bradycardia and reduced cardiac output
(Stevens et al., 1972
;
Farrell, 1982
;
Farrell and Jones, 1992
), and
would also result in hypoperfusion if increased intramuscular pressure
compresses the supplying segmental arteries. Even so, the fact that mean
PRMO2 did not decrease below
40
mmHg is a novel finding indicating that RM remained well supplied with oxygen
during spontaneous struggling behaviours in rainbow trout. These observations
suggest that the previously observed precipitous decrease in
PvO2
(Farrell and Clutterham, 2003
)
during struggling is driven by tissues in addition to RM, the most likely
candidate being the WM.
Another novel finding of the present study is that the
PRMO2 of approximately 60 mmHg
measured in the free-swimming normoxic trout is appreciably higher than the
PO2 of 24 mmHg measured with
microelectrodes in the WM of eels
(Jankowsky, 1966).
Unfortunately, this earlier study does not detail exactly how the probes were
implanted and whether the eels were conscious during subsequent measurements
(Jankowsky, 1966
). Therefore,
given our observation of a low PRMO2
during anaesthesia, further studies with WM are warranted to confirm this
difference between RM and WM. In contrast, it is very clear that the normoxic
PRMO2 in rainbow trout is
significantly higher than in the skeletal muscle of mammals, where
PO2 values measured with implanted
microelectrodes range from 25 mmHg to 35 mmHg in conscious humans Homo
sapiens (Jung et al.,
1999
; Suttner et al.,
2002
) and dogs Canis canis
(Hutter et al., 1999
). Similar
values were obtained in anaesthetised rats Rattus norvegicus, using
phosphorescence quenching techniques
(Behnke et al., 2001
). In view
of this difference, we provide the first direct evidence to support the
earlier suggestions by Egginton
(2002
) that the anatomy and
physiology of RM in teleost fish could lead to an elevated
PO2 compared with mammals.
If the PO2 in respiring tissues is
determined by the rate at which O2 is supplied in the blood, the
distance and speed it diffuses, and the rate at which the tissue consumes it
(Egginton, 2002), then a
comparison of these variables between teleost RM and skeletal muscles of
mammals might provide insight into why
PRMO2 is so high. Mass-specific
blood flow rates to trout RM may be up to twice the level reported for
mammalian skeletal muscles at rest, although they are similar during exercise
(Egginton, 1987
,
2002
;
Taylor et al., 1996
). Rainbow
trout haemoglobin has a similar affinity for O2 to that of, for
example, humans and rats (Wilmer et al.,
2000
). Egginton
(2002
) calculated and compared
the mean geometric supply area (domain of influence) as well as the mean
Krogh's diffusion distance for capillaries in the tibialis anterior (TA) of
both rats and Syrian hamsters Mesocritus auratus versus those in the
RM of both rainbow trout and striped bass Morone saxatilis. In these
two teleosts, domains and diffusion distances were approximately 20% smaller
than in the hamster, whereas rat domains were approximately eightfold larger
and diffusion distances approximately twofold larger than in the other three
species (Egginton, 2002
). Thus,
the higher blood flow and smaller capillary domains clearly favour a higher
PO2 in the red muscle of the rainbow trout
relative to the skeletal muscles of the rat
(Behnke et al., 2001
). The
lower body temperature of the fish, however, will lead to a significant
reduction in O2 diffusivity, an effect that is only partially
offset by a concurrent reduction in tissue O2 consumption
(Taylor et al., 1997
;
Egginton, 2002
).
Insights into red muscle O2 supply during graded exercise
Our measurements of PRMO2 in fish
during graded exercise, at exhaustion and during recovery are also novel.
Furthermore, it is evident that they contrast with results in exercising
mammals. In both conscious humans and the anaesthetised rat, sustained
exercise reduces intramuscular PO2 from around
30 mmHg to below 20 mmHg, a change that is attributed to increased rates of
O2 extraction by the working muscle
(Jung et al., 1999;
Behnke et al., 2001
). The
significant decrease in PRMO2 during
sustained exercise in the current study presumably occurred for the same
reason. However, PRMO2 declined to
only 45 mmHg at the maximum rates of exercise performance and
O2, which is
considerably higher than the PO2 values
observed in mammals (Jung et al.,
1999
; Behnke et al.,
2001
). Egginton et al.
(2000
), using morphological
data and analysis of the resulting physico-chemical conditions for
O2 diffusion, estimated that the PO2
gradient between capillaries and the centre of a red muscle fibre may be less
than 4 mmHg in trout at maximum sustained exercise. Thus, the high
PRMO2 suggests that rainbow trout RM
may not become hypoxic at high levels of sustained exercise, a suggestion that
is supported by two other lines of evidence. First, resolution of the Fick
equation revealed that the reduction in the arterial to RM
PO2 gradient that occurred between a swimming
speed of 0.5 BL s1 and maximal exercise would have
required an approximately fivefold increase in blood supply to meet the
measured increase in
O2. This
increase compares favourably with the eightfold increase in blood supply to RM
measured with microspheres during maximum sustained exercise in rainbow trout
(Taylor et al., 1996
). Second,
at exhaustion PRMO2 increased rather
than decreased. This contrasts with tetrapod skeletal muscles, where fatigue
is associated with a profound decline in PO2 to
below 50% of resting values (Molé
et al., 1999
; Howlett and
Hogan, 2001
). This suggests that when WM is recruited to power
swimming speeds above 70% of Ucrit
(Burgetz et al., 1998
;
Lee et al., 2003
) subsequent
exhaustion is not linked to major reductions in RM O2 supply.
Consequently, convective O2 supply to the RM seems not to be a
limiting factor for maximum aerobic performance in rainbow trout. Prolonged
exercise at 90% of Ucrit leads to depletion of oxidative
substrates in trout RM (Richards et al.,
2002
), so this may be the cause of fatigue. Alternatively, RM may
simply reduce its activity when WM is recruited during incremental exercise, a
gait transition representing an orderly and necessary transition to a muscle
that can generate the required increase in tailbeat frequency and muscular
power output (see Jones and Randall,
1978
). One consequence of this gait transition is that
PRMO2 remains high, higher than
PvO2 at fatigue
(Farrell and Clutterham,
2003
). Further research into this area is clearly required, not
least to determine the validity of an incremental graded exercise protocol in
investigating factors limiting maximum rates of aerobic metabolism and
performance in fish.
Insights into the impact of the Root effect upon red muscle O2 tensions
There was no evidence that the Root effect influenced tissue O2
tension enough to raise PRMO2 above
PaO2 in the rainbow trout. In fact, the
opposite was always true, both in normoxia and in mild hypoxia, when the
PaO2 to
PRMO2 gradient was reduced. Indeed,
PRMO2 was sensitive to changes in
PaO2 and although the proportional changes in
PRMO2 during hypoxia were
significantly less than the changes in PaO2,
this could be attributed to the sigmoid shape of the trout
HbO2 dissociation curve. Thus, as
PaO2 declined, the arterial to RM
PO2 difference shifted left towards the steep
portion of the dissociation curve, such that a smaller drop in
PO2 was required to elicit the same degree of
O2 unloading.
In addition to PRMO2 being
elevated compared with measurements in mammalian muscles, it is interesting
that PRMO2 was also consistently
higher than published values for mixed PvO2 in
the trout, both in normoxia and at comparable degrees of hypoxia
(Holeton and Randall, 1967;
Farrell and Clutterham, 2003
).
Indeed, the measured values for
PRMO2 lie almost exactly midway
between published values for PaO2 and
PvO2 at the appropriate water
PO2
(Holeton and Randall, 1967
).
In contrast, the reported range for mammalian intramuscular
PO2 (Hutter
et al., 1999
; Jung et al.,
1999
; Behnke et al.,
2001
; Suttner et al.,
2002
) is consistently lower than that of mixed
PvO2, which is typically around 40 mmHg
(Hutter et al., 1999
;
Wilmer et al., 2000
). The
higher PRMO2 relative to
PvO2 in the trout can be interpreted in one of
two ways. One possibility is that venous return from RM is a relatively small
contribution to mixed venous blood. The other possibility is that the high
PRMO2 of rainbow trout relative to
mammals could be, at least in part, a consequence of a Root effect in blood
perfusing the RM. The Root effect would be engendered by transient changes in
erythrocyte pH caused by the faster rates of CO2 diffusion than
O2 diffusion, and the strong coupling of O2 and
CO2 movements that are known to exist in trout blood
(Brauner and Randall, 1998
;
Brauner et al., 2000
). That is,
when arterial blood enters the RM of trout, rapid diffusion of metabolic
CO2 into the erythrocyte would cause a transient drop in pH and
cause a Root `off-shift', driving O2 off the haemoglobin and
raising PO2. The deoxygenated haemoglobin
would, however, then bind protons (the Haldane effect) and cause blood pH to
rise again, eliciting a Root `on-shift' that binds O2 back onto the
haemoglobin and lowers PO2 in the venous blood
leaving the tissue.
While such a role of the Root effect is conjecture at this time, we can
eliminate the possibility that we measured an artefact of mixed arterial,
tissue and venous PO2 values rather than
intramuscular PO2 If this had been the case,
PRMO2 should have varied directly
with PaO2 during hypoxia and exercise, which it
did not. Furthermore, similar concerns would, presumably, exist for mammalian
studies of intramuscular PO2 that involved the
implantation of microelectrodes (Hutter et
al., 1999; Jung et al.,
1999
; Suttner et al.,
2002
). Thus, in addition to the anatomical reasons for elevated
PRMO2 that have been raised by
Egginton (2002
), the current
study has not eliminated the possibility that O2 tensions are also
influenced by the action of the Root effect within the muscle vasculature.
Future investigations should perhaps be aimed at experimental manipulation of
the Root effect to investigate how this change influences
PRMO2 relative to
PaO2 and mixed
PvO2.
Conclusions
The results show that the PO2 prevailing in
the RM of rainbow trout is higher than that reported for skeletal muscles of
rats and humans. While there was a significant decrease in
PRMO2 during sustained exercise, it
did not decline below 40 mmHg and increased slightly at exhaustion. These
observations are taken as a strong indication that O2 supply to the
RM does not become limiting either at the moment of recruitment of WM or at
exhaustion. We found no dramatic evidence that the Root effect raises
O2 tensions in red muscle because
PRMO2 remained almost exactly midway
between previously published values of PaO2 and
PvO2 for rainbow trout and was sensitive to
reductions in PaO2 during mild hypoxia. Further
work is needed to explain the higher PO2 in the
RM relative to mixed venous blood because, while this may reflect a limited
contribution from RM to mixed venous return, the phenomenon might also be a
consequence of a transient Root effect in the RM vasculature.
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Acknowledgments |
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References |
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