EFFECTS OF HIGH INTENSITY EXERCISE TRAINING ON CARDIOVASCULAR FUNCTION, OXYGEN UPTAKE, INTERNAL OXYGEN TRANSPORT AND OSMOTIC BALANCE IN CHINOOK SALMON (ONCORHYNCHUS TSHAWYTSCHA) DURING CRITICAL SPEED SWIMMING
1
Continuing Studies in Science, Simon Fraser University, Burnaby, BC, V5A
1S6, Canada
2
Department of Biological Sciences, Simon Fraser University, Burnaby, BC,
V5A 1S6, Canada
3
Holar Agricultural College, 551 Sudarkrokur, Iceland
4
Department of Fisheries and Oceans, West Vancouver Laboratory, West
Vancouver, BC, V7V 1N6 Canada
*
Present address: Matre Research Station IMR, 5198 Matredal, Norway
Author for correspondence (e-mail:
farrell{at}sfu.ca
)
Accepted May 14, 2001
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Summary |
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Key words: salmon, cardiac output, heart rate, oxygen consumption, plasma osmolality, oxygen transport, swimming, exercise training, osmorespiratory compromise, Oncorhynchus tshawytscha
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Introduction |
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Earlier, Davison (Davison,
1989) concluded that the
evidence for training-induced improvements in internal oxygen transport
capacity and swimming performance is equivocal, largely because the magnitude
of many of the reported changes was small. It is also possible that the
exercise training regimens used in previous studies were not always of a
sufficient intensity or duration to elicit cardiovascular change.
Consequently, we used a high-intensity exercise-training regimen over a
4-month period in an attempt to elicit a maximum cardiorespiratory response
before measuring cardiorespiratory performance during a critical swimming
speed test.
We also explored the possibility that exercise training can provide
benefits beyond those that directly benefit locomotory performance. During
swimming in sea water (SW), ionic and osmotic balance are disrupted (Rao,
1968; Rao,
1969
; Farmer and Beamish,
1969
; Byrne et al.,
1972
; Wood and Randall,
1973a
; Wood and Randall,
1973b
; Webb,
1975
; Febry and Lutz,
1987
) because the functional
surface area of the gills (Booth,
1979
; see also Wood and Perry,
1985
) and the permeability of
the gills to ions (Gonzalez and McDonald,
1992
; Gonzalez and McDonald,
1994
) both increase. This
enhanced diffusional exchange of gases, ions and water with the environment is
the so-called `osmo-respiratory compromise' (Randall et al.,
1972
; Nilsson,
1986
), which has been
well-studied in freshwater (FW) fish (Gonzalez and MacDonald,
1992
; Gonzalez and MacDonald,
1994
). In resting rainbow
trout, for example, the estimate is that one sodium ion is lost across the
gills for every eight molecules of oxygen taken up. However, when
o2max increases
during exercise, sodium loss is enhanced more than
o2 such that one
sodium ion is lost for every five molecules of oxygen taken up (Gonzalez and
MacDonald, 1992
). In contrast
to FW fish, the relationships between osmoregulatory capacity, swimming
performance and
o2max have not
been well investigated in SW salmon, especially with respect to training
effects. Ionic/osmotic inbalances have been linked, however, to reductions in
aerobic swimming performance in juvenile salmonids (Houston,
1959
; Brauner et al.,
1992
). Our working hypothesis,
given the osmorespiratory compromise, was that exercise-trained fish
with a higher aerobic capacity would be better able to manage the metabolic
costs of ionic and osmotic regulation while swimming.
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Materials and methods |
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Surgical procedures
On the day before surgery, fish were individually transferred to a 201
indoor holding tank continuously flushed with SW at 9-10°C. Fish were
anaesthetised in a chilled solution of 2-pheoxyethanol in SW (1:2,000) and
placed supine on an operating sling. Anaesthesia was maintained by
continuously irrigating the gills with a solution of 2-phenoxyethanol in
chilled SW (1:4,000). A cannula (PE50, Clay Adams, Parsippany, NJ, USA) was
inserted into the dorsal aorta (DA) as described by Thorarensen et al.
(Thorarensen et al., 1993) and
modified from Soivio (Soivio,
1975
). The cannula was
externalised through the thin skin membrane under the maxillary and filled
with heparinised (150 i.u. ml-1) saline (0.9 % NaCl). This cannula
was used for sampling arterial blood and measuring arterial blood pressure
(Pda). A pulsed Doppler flow probe (TMI, Iowa City, IA,
USA) was placed around the ventral aorta, just distal to the bulbus
arteriosus, to provide a continuous measurement of
(cardiac output; total blood flow in
the ventral aorta). The flow probes were made with rigid plastic collars and
selected to fit snugly around the vessel. The ventral aorta was accessed via
the opercular cavity (Steffensen and Farrell,
1998
). A 3-5 mm segment of the
vessel was teased free from the surrounding tissue without rupturing the
pericardium or obstructing the coronary artery. Silk thread (3-0) was used to
suture the leads from the probe to the isthmus and to the side of the fish,
behind the cleithrum and just under the lateral line. The leads and the
cannula were also anchored in front of the dorsal fin. The entire operation
lasted less than 20 min. The fish were allowed to recover for 4-5 h in a 201
tank and then overnight in a swim tunnel. The total recovery time before
experimentation commenced was 24 h. Body mass was measured immediately before
transfer to the swim tunnel.
Experimental protocol
The critical swimming test involved incremental velocity steps in a
Brett-type swim tunnel. Ucrit (cm s-1 or
BL s-1) and
o2 were measured
using methods described previously (Thorarensen et al.,
1993
; Gallaugher et al.,
1995
). Before the fish started
swimming, routine
,
Pda and
o2 values were
recorded and an arterial blood sample was taken. Swimming speed was then
increased to 1 BL s-1 and the sampling procedure was
repeated. Subsequently, swimming velocity was increased in steps of 0.25
BL s-1, each step being maintained for 20 min.
, Pda and
o2 were recorded
at each velocity increment after the fish reached a steady state, i.e.
approximately 8-10 min after the velocity was increased. As the fish
approached Ucrit (as indicated by `burst and coast'
swimming behaviours in the otherwise steady swimming pattern), a blood sample
was taken at each water velocity step. Blood samples at
Ucrit were always drawn while the fish was swimming, which
in some cases required a reduction of water velocity by one step (see
Gallaugher et al., 1992
).
After fatigue,
,
Pda and
o2 were recorded
following a 1 h recovery period. Consequently, all cardiorespiratory variables
were measured under resting conditions, while the fish swam at 1 BL
s-1, at 80% Ucrit, at 100%
Ucrit and after a 1 h recovery period. Under resting
conditions and during recovery, the water velocity was just sufficient to keep
the fish orientated into the water current but stationary on the bottom of the
swim tube. After the experiment, fish were anaesthetised to calibrate the flow
probe and then sacrificed with a blow to the head prior to body mass and heart
mass being measured. Relative ventricle mass (RVM) was calculated as
100xventricle mass/body mass. All procedures were in accordance with the
Canadian Council on Animal Care and approved by Simon Fraser University.
Blood sampling and analytical techniques
For each 1.0 ml arterial blood sample, arterial O2 tension
(PaO2) and arterial O2 content
(CaO2), arterial pH (pHa), hematocrit (Hct), hemoglobin
concentration ([Hb]) and plasma osmolality were determined. Plasma lactate
concentration [La] was measured only at rest, at Ucrit and
during recovery. To prevent anemia as a result of the repetitive blood
sampling, 1.0 ml of blood, made up from blood used to measure
PaO2 and pHa, any remaining blood from the sample and
blood from a normocythemic donor fish, was returned to the experimental fish
via the DA cannula.
Measurements of PaO2 were made using a Radiometer
(Copenhagen) E5046 Po2 electrode in a D616 cell
and whole blood pHa was determined on samples injected into a Radiometer pH
microelectrode (type E5021). Both electrodes were regulated at the
experimental water temperature and linked to a Radiometer PHM71
acidbase analyzer. A second oxygen electrode system was used to measure
water Po2. CaO2 was
measured in 30 µl blood samples using the method of Tucker (Tucker,
1967). Hct was measured in
triplicate (20 µl samples drawn into microcapillary tubes) using a
Haemofuge (Heraeus Sepatech, Netherlands) centrifuge (10,000 g
for 3 min). Sigma diagnostic kits (Sigma Chemical Co., St Louis, MO, USA) were
used to measure blood [Hb] (no. 525A) in 20 µl blood samples and [La] (no.
826-UV) in 100 µl plasma samples. Mean cell hemoglobin concentration (MCHC)
was calculated as [Hb]/Hct. Plasma osmolality was measured in triplicate on 10
µl samples using a Wescor (5100) Vapour Pressure Osmometer (Wescor, Logan,
UT, USA).
Measurements of muscle dry matter
Analyses of muscle dry matter and ash content were performed on separate
samples of control (N=20) and exercise-trained fish (N=20)
at the end of their exercise training. Similar analyses were performed for
control (N=8) and exercise-trained (N=8) fish after the 1 h
recovery from the Ucrit swim test. These analyses involved
drying tissue at 100°C for 16-18 h (muscle dry matter, % of tissue wet
mass) or 3 h at 600°C (ash content, % of tissue wet mass), as described by
Kiessling et al. (Kiessling et al.,
1994a).
Possible effects of surgery on oxygen consumption and critical
swimming performance
To determine if osmotic disruption during swimming was in some way
influenced by tissue damage associated with the placement of the Doppler flow
probes, a separate group of exercise-trained fish (N=6) received only
a DA cannula for the Ucrit test in the swim tunnel. In
addition, o2max
was measured in separate groups of exercise-trained and control fish that had
not been cannulated, and this allowed us to assess the effects of the Doppler
flow probe and cannulation procedures.
Calibration of flow probes
Doppler flow probes measure relative changes in
. Therefore, each probe was calibrated
in situ at the end of the Ucrit experiment with
the fish re-anaesthetised. To do this, a Transonic flow probe (Transonic Inc.,
Ithaca, NY, USA), which measures absolute blood flow, was placed around the
bulbus and ventral aortic flow was recorded simultaneously from the Doppler
and Transonic flow probes. (Transonic flow probes were not used for the
experiments because of their rather larger size. The smaller Doppler flow
probes were less likely impair swimming in these fish weighing 300-400 g.)
Doppler flow probes were successfully calibrated in six fish from each group.
Experiments were attempted on 14 fish for each group, but in some cases the
flow probe was not successfully calibrated and in others either blood pressure
or hematology measurements were missing. For statistical purposes, only fish
that had all variables measured successfully were included in the
cardiovascular data analysis. Variables that were measured and not included
below were in general agreement with the overall findings.
Data acquisition and measurements of cardiorespiratory variables
Pda was measured with a LD15 pressure transducer
(Narco, Houston, TX, USA) connected to a Grass preamplifier (Model 791J, Grass
Instruments, Quincy, MA, USA). The pressure transducer was calibrated daily
and regularly referenced to the water level in the swim tunnel during the
experiment. The signals from the flow meter, pressure transducer and the
oxygen meter were amplified by a Grass chart recorder (Model 7PCP B, Grass
Instruments Quincy, MA, USA) and stored by a computer. The computer sampled
signals for blood flow and blood pressure at a rate of 5 Hz. Variables were
measured for 6 min and then averaged. Labtech Notebook software (Laboratory
Technology Corp., Wilmington, MA, USA) was used to process the signals and to
calculate heart rate, fH.
Calculations of oxygen extraction and systemic vascular
resistance
Compared with our experience with rainbow trout, chinook salmon were less
tolerant of extensive surgery. Therefore, rather than adding a second cannula
to sample venous blood for direct measurements of
Eo2, we decided to calculate
Eo2 as a percentage using the Fick equation
(Eo2=100[o2/(
xCaO2)]). To preclude possible errors associated
with tissue utilisation of oxygen directly from the water, this calculation
was only performed at
o2max. While the
net amount of oxygen delivered to the tissues by the cardiovascular system is
equal to
o2xEo2,
tissues such as the skin and the gill epithelia can utilise oxygen directly
from the water (Kirsch and Nonnotte,
1977
; Daxboeck et al.,
1982
). Even so, the
contribution of this form of oxygen delivery is considered to be minimal when
salmonids approach
o2max (Neuman et
al., 1983
; Thorarensen et al.,
1996
; Brauner et al.,
2000a
). Systemic vascular
resistance (Rsys) was calculated from
Rsys=Pda/
and the small effect of venous blood pressure on Rsys was
disregarded.
Statistics
Mean values ± S.E.M. are presented throughout the text and figures
and the fiducial limit for accepting significance was P<0.05.
There was variability in individual swimming performance and therefore
swimming speed was normalised to %Ucrit to assist in some
comparisons. All variables were compared with a three-way ANOVA with
individuals, swimming velocity and training level as factors. Mean levels at
each swimming speed were compared with a least-square estimate. Statistical
comparisons of hematological variables at rest, 1 BL s-1,
approx. 80% Ucrit, Ucrit and during
recovery were made between control and exercise-trained groups using a
repeated-measures ANOVA. Changes in hematological variables within each group
were analyzed by a paired t-test for means. The other variables
reported here were statistically analysed using the GLM procedure in SAS
(Version 6, SAS Institute Inc., Cary, NC, USA). A significant difference
between the control and exercise-trained fish was regarded as a training
effect.
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Results |
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Effect of swimming and training on heart mass and cardiovascular
variables
Relative ventricular mass was significantly larger in the exercise-trained
fish (0.114±0.003, N=12) compared with control fish
(0.101±0.003, N=12). Although the heart mass of
exercise-trained fish was larger, was
not significantly different between exercise-trained and control fish at any
swimming velocity (Table 1,
Fig. 2A). Routine
was 35.8 ml min-1
kg-1 and 33.6 ml min-1 kg-1 for the control
and exercise-trained groups, respectively, and with swimming,
increased by 94% and 83% to maximum
values of 65.5 and 65.1 ml min-1 kg-1, respectively
(Table 1).
max was recorded at
swimming velocities of 90±6% and 94±1% of
Ucrit for control and exercise-trained fish, respectively.
While routine
and
max were the same in both
groups of fish, VSH and fH increased
somewhat differently. At the lower swimming speeds, exercise-trained fish
increased VSH (Fig.
2E) to a greater degree than control fish
(Fig. 2D). Even so, >60% of
the total increase in
associated with
critical swimming had occurred at a velocity of 1 BL s-1
in both groups of fish (Fig.
2A). At Ucrit, VSH
increased by 61-65% and fH by 10-22%
(Table 1).
|
There was no significant change in PDA with increased swimming velocity in exercise-trained fish, but PDA increased significantly for control fish (Fig. 2G). The significantly lower PDA for exercise-trained fish came about because Rsys decreased significantly, whereas Rsys did not change significantly in control fish.
Effect of swimming and training on hematological variables
Hematological variables are compared in
Table 2. Hct, [Hb], MCHC and
CaO2 did not change significantly with swimming velocity
in either group, nor were they significantly different following the 1 h
recovery (Table 2). However,
swimming induced an arterial hypoxemia in both groups of fish because
PaO2 was significantly reduced at all swimming velocities
and during recovery.
|
Small, but statistically significant training effects were observed for some hematological variables (Table 2). The overall mean values for Hct, [Hb], and MCHC were significantly higher in exercise-trained fish (Table 2). Also, the extent of the arterial hypoxemia at Ucrit was significantly greater for exercise-trained fish (Table 2). Nevertheless, CaO2 was unaffected by high-intensity exercise training.
Changes in plasma [La] and pHa during swimming were similar for control and exercise-trained fish. Plasma pHa was decreased significantly at all swimming velocities and during recovery (Table 2). Plasma [La] increased significantly at Ucrit and increased further still during recovery. However, plasma [La] values were not significantly different between control and exercise-trained fish and were, respectively, at rest: 0.4±0.1 mmoll-1 (N=5) and 0.8±0.2 mmoll-1 (N=9); at Ucrit: 3.6±0.4 mmoll-1 (N=6) and 3.0±0.4 mmoll-1 (N=8): after the 1 h recovery: 4.6±0.7 mmoll-1 (N=6) and 5.1±0.8 mmoll-1 (N=8).
Effect of swimming and training on arterial oxygen transport.
The measured variables associated with arterial oxygen convection are
summarised in Table 1.
o2 increased
during swimming because
increased,
while CaO2 was unchanged. High-intensity exercise training
did not have a significant effect on
o2
(Fig. 2B); neither
max nor
CaO2 was significantly different between control and
exercise-trained fish. The recovery from fatigue did not differ between
control and exercise-trained fish in that the recovery values for
o2,
, Rsys and
o2 were not
significantly different from routine values
(Fig. 2). However,
fH was significantly higher and PDA
was significantly lower than the pre-exercise values in the exercise-trained,
but not the control group.
Given that exercise training increased
o2max and not
o2, the
improvement in oxygen delivery to tissues came about through an increase in
Eo2. At
o2max the
calculated Eo2 for exercise-trained fish (90%)
was significantly greater than for the control group (62%)
(Table 1). Furthermore, because
and
o2 had increase
by 50% at low swimming velocities and there was little change in
o2 until fish
were swimming at a velocity close to 60-80% of Ucrit
(Fig. 2), it is likely that
Eo2 decreased at low swimming velocities.
Effect of swimming and training on water balance
Control and exercise-trained fish lost a similar amount of body water while
swimming to the same Ucrit. Body mass decreased
significantly by 8% and 5% in control and exercise-trained fish, respectively
(Table 3). A similar amount
(5%) of water loss occurred in the fish that had received only a DA cannula
(Table 3) and so water loss was
not significantly affected by implanting a Doppler flow probe. The loss of
body water was reflected in an increase in plasma osmolality. Compared with
routine values, plasma osmolality increased significantly at approx. 80%
Ucrit, Ucrit and after the 1 h
recovery period in both groups of fish
(Fig. 4). In addition, both
muscle dry matter (Fig. 3) and
ash content (1.75±0.03%, N=8) increased significantly
following exercise, compared with fish sampled directly from the training
tanks.
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Exercise-trained fish had a significantly greater muscle dry matter
(Fig. 3) and ash
(1.56±0.03%, N=20 versus 1.51±0.03%,
N=20) compared with control fish. In addition, exercise-trained fish
were significantly better at defending their plasma osmolality during exercise
(Fig. 4A). Plasma osmolality
was significantly lower in exercise-trained fish compared with control fish at
approx. 80% Ucrit and at Ucrit. Plasma
osmolality at rest and after a 1 h recovery period, however, was not
significantly different between control and exercise-trained fish
(Fig. 4A). In view of this
finding, we measured plasma omolality in stored samples from fish used in our
earlier study that employed a less intense training regimen with chinook
salmon (Thorarensen et al.,
1993). As in the present
study, trained fish were better at defending plasma osmolality during swimming
(Fig. 4B).
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Discussion |
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Effects of exercise training on internal oxygen convection
We are the first to comprehensively measure the cardiorespiratory changes
associated with chronic, high-intensity exercise training in fish and to
delineate the resultant cardiorespiratory benefits. The exercise-training
regimen used here produced a clear improvement in
o2max. However,
this change did not directly benefit locomotory performance in terms of
improving Ucrit and there was no training effect on
o2max. Given the
increase in
o2max, we
anticipated that CaO2 would increase beyond the level
observed previously with a lower intensity exercise regimen (continuous
exercise training at 1.5 BL s-1, which represented about
60% Ucrit or 40%
o2max, increased
Hct, [Hb] and CaO2; Thorarensen et al.,
1993
). Instead, we observed
smaller training effects on Hct and [Hb] and no training effect on
CaO2. This result, coupled with the fact that
o2max,
Ucrit and
o2max can all be
altered with experimental blood doping in SW rainbow trout (Gallaugher et al.,
1995
), suggests that a routine
Hct (32.3%) may be near an upper limit for chinook salmon under these
environmental conditions. As in previous studies (Gallaugher et al.,
1992
; Thorarensen et al.,
1993
; Gallaugher et al.,
1995
), we also observed
arterial hypoxemia at Ucrit. However, the extent of this
arterial hypoxemia was greater in the exercise-trained group. This training
effect might be related either to the somewhat higher Hct in exercise-trained
fish (arterial hypoxemia in rainbow trout was reported to be Hct-dependent;
Gallaugher and Farrell, 1998
),
or to a lower venous oxygen content in exercise-trained fish. Despite an
intensified arterial hypoxemia with swimming, CaO2 was
unaffected in exercise-trained fish.
Like CaO2,
max was unaffected by
intense exercise training. Therefore,
O2max improved
because exercise training improved EO2 rather
than
O2max. The
calculated EO2max increased from 65% in control
fish to 90% in exercise-trained fish. Although
EO2max was calculated and probably should be
confirmed with direct measurements in future work, our calculations are in
line with values reported for other fish species and mammals. For example,
EO2max in exercising rainbow trout was between
65% and 85% at Ucrit (Kiceniuk and Jones,
1977
; Brauner et al.,
2000a
; Brauner et al.,
2000b
). Similarly, in
exercising mammals EO2max is typically 60-80%
(Taylor et al., 1987
; Jones et
al., 1989
; Longworth et al.,
1989
; Piiper,
1990
), but can reach 80-90% in
muscles during relatively short periods of intense exercise (Richardson et
al., 1993
). That
EO2max is plastic and can respond to training
is a novel finding for fish. Thus, intraspecific cardiovascular plasticity
that enhances
O2max in
response to training clearly contrasts with the interspecific adaptations in
max and
CaO2 that produce species differences in
O2max.
Greater oxygen extraction at the tissues is perhaps not entirely unexpected
as a training response, given that exercise training is known to improve
capillarity in fish muscles (Davie et al.,
1986;
Sänger,
1992
). Although capillary
density was not measured in our fish, two lines of indirect evidence suggest
that muscle capillarity could have increased with exercise training. First,
the cross-sectional area of the red locomotory muscles, which have a better
capillary supply compared to white muscle (Egginton,
1992
), was shown to increase
relative to that of white muscles in fish with the same training regimen
(Kiessling et al., 1994b
).
Second, the lower Rsys at Ucrit in the
exercisetrained group is consistent with more capillary beds being perfused
simultaneously. Some of these could be in the skeletal muscle, although a
higher intestinal blood flow during swimming (see below) also could contribute
to a lower Rsys. Increased capillarity increases the
diffusional surface area for oxygen and reduces the mean distance between
capillaries and mitochondria, both of which would increase oxygen conductance
(Weibel et al., 1992
). Red
skeletal muscle in skipjack tuna is characterised by a high capillary density,
a small fibre size and a high mitochondrial volume density (Mathieu-Costello
et al., 1992
; Mathieu-Costello
et al., 1996
). In addition,
capillary manifolds are present in tuna red muscle and these manifolds
increase venular capillary surface area, favouring increased oxygen extraction
by the muscle. Increased capillarity also increases the mean capillary transit
time of red blood cells, even if
max is unchanged, and so
more time is available for the unloading of oxygen. Transit time has been
implicated as one of the limitations to oxygen extraction from blood in
mammals (Saltin, 1985
). In
addition to capillary changes, an increase in muscle myoglobin concentration
could increase EO2max. Exercise training is
known to increase muscle myoglobin concentrations (Love et al.,
1977
) and myoglobin is also
known to facilitate oxygen transport within the muscle fibres (Gayeski et al.,
1985
; Bailey and Driedzic,
1986
).
The above findings all point to oxygen diffusion between the capillaries
and the mitochondria being a significant limiting factor, i.e. the
cardiorespiratory system in salmonids may be diffusion-limited rather than
perfusion-limited during exercise. This would then explain why exercise
training affected EO2max rather than
O2max in chinook
salmon. A training-induced increase in the diffusive surface area of
capillaries, the residence time of blood in capillaries, or a
myoglobin-mediated facilitated diffusion of oxygen in muscle cells could all
have contributed to a higher EO2max during
swimming. This suggestion that oxygen transfer to the tissues is
diffusion-limited during exercise in salmon is consistent with the results of
blood-doping experiments in rainbow trout. Gallaugher et al. (Gallaugher et
al., 1995
) found that while
blood doping could be used experimentally to improve
O2max, the
benefits to either
O2max or
Ucrit were rather small whenever Hct was artificially
increased above its routine level. Diffusion limitations for oxygen transfer
at the gills, however, do not appear to be as severe as at the tissues because
CaO2 was maintained in spite of the
swimming-induced arterial hypoxemia, and oxygen transport to the tissues was
not adversely affected.
A large proportion of the salmonid heart muscle relies on venous blood for
its oxygen supply (Farrell,
1992; Steffensen and Farrell,
1998
). Therefore, a potential
problem associated with an increase in EO2max
is that the reduction in the amount of oxygen in venous blood might impair
myocardial oxygen supply during swimming. Even so, this problem may have been
ameliorated in trained chinook salmon because
max was unchanged and
PDA was lower in exercise-trained fish. Hence, myocardial
oxygen demand, which is directly related to myocardial power output, may have
been lower in trained fish. Furthermore, a training effect on the coronary
supply to the heart could help alleviate the problem of lower venous oxygen
content. We found that relative ventricular mass was plastic and responded to
exercise training, albeit in a limited manner. The 10% increase in relative
ventricular mass is consistent with the 12% observed earlier by Hochachka
(Hochachka, 1961
), but lower
than the unusual 46% increase observed by Greer Walker and Emerson (Greer
Walker and Emerson, 1978
).
Nevertheless, several studies report only isometric cardiac growth with
exercise training (see Farrell et al.,
1990
for references). How
cardiac remodelling might relate to changes in myocardial oxygen supply and
the coronary circulation is unclear.
Effects of exercise training on swimming performance and osmotic
balance
Exercise-training effects on Ucrit are equivocal. For
example, several authors have observed positive training effects on
Ucrit (Nahhas et al.,
1982; Besner and Smith,
1983
; Farrell et al.,
1990
), but in all cases the
improvement in Ucrit was rather small (<20%). In
contrast, no training effect on Ucrit was observed in
either rainbow trout (Farrell et al.,
1991
) or chinook salmon
(Thorarensen et al., 1993
;
this study). Undoubtedly, the different responses among training studies
reflect, in part, important differences in the intensity and duration of the
exercise-training regimens that have been used in the past, as well as in the
level of exercise that the control fish were subjected to. We found no effect
of cannulation on Ucrit, while others have reported that
cannulae reduce Ucrit in rainbow trout (e.g. Kiceniuk and
Jones, 1977
). We have no
explanation for this but there are a number of possibilities. Firstly, our
fish were not held stationary in the holding tanks and this may have increased
the overall exercise capabilities of the fish. Secondly, chinook salmon have
not been held under culture conditions that select for growth rather than
athleticism for as many generations as have rainbow trout. Also, surgical
techniques have improved over time and this may have minimized the impact of
cannulation procedures in more recent studies.
If salmon do not swim much faster when exercise-trained, even when the training regimen is high intensity and for long periods, what then are the benefits of exercise training? Below, we present the idea that exercise-training lessens the osmorespiratory compromise during swimming.
With swimming and the attendant improvement in gas exchange at the gills,
it is well established that there is a somewhat greater and disruptive effect
on passive ion movements across the gills of FW fish (Gonzalez and MacDonald,
1992; Gonzalez and MacDonald,
1994
). Numerous studies have
shown that, as a result of swimming, teleosts dehydrate in SW and hydrate in
FW (e.g. Rao, 1969
; Farmer and
Beamish, 1969
; Byrne et al.,
1972
; Wood and Randall,
1973a
; Wood and Randall,
1973b
). We used plasma
osmolality and tissue water content as measures of osmoregulatory performance
during swimming and the changes we observed in SW chinook salmon are
consistent with progressive dehydration. Besides the gills, the gut is an
important osmoregulatory organ in SW in that it is responsible for the water
uptake that counteracts the passive water loss occurring across the gills.
Therefore, for dehydration to occur during swimming, water loss via
the gills must exceed water absorption via the intestine. The exact
mechanisms by which this imbalance comes about are unknown, but a decrease in
gut blood flow could certainly play a role by impairing intestinal water
absorption, adding to the problem of increased diffusional losses at the
gills. Normally, when fish swim or struggle, gut blood flow decreases
(Thorarensen et al., 1993
;
Farrell et al., 2001
),
presumably as a mechanism to divert blood flow to locomotory muscles (Randall
and Daxboeck, 1982
;
Thorarensen et al., 1993
).
Nevertheless, exercise-trained chinook salmon are better able to defend
intestinal blood flow during swimming (Thorarensen et al.,
1993
). Consequently, the
finding here, as well as in our earlier study (Thorarensen et al.,
1993
), that exercise-trained
chinook could defend their plasma osmolality while swimming better than
control fish, might be explained, in part, by better gut blood flow and water
uptake during exercise.
We propose that the higher
O2max values of
the exercise-trained fish, in part, reflect an osmoregulatory cost that
enabled plasma osmolality to be better maintained despite elevated water loss
across the gills. However, exactly what this osmoregulatory cost might be in
active fish is difficult to ascertain because estimates are highly variable
(see Morgan and Iwama, 1991
).
Using data from Rao (Rao,
1968
) and Farmer and Beamish
(Farmer and Beamish, 1969
),
Webb (Webb, 1975
) estimated an
osmoregulatory cost of approx. 16% of the net cost of swimming at
Ucrit for SW-adapted adult rainbow trout and tilapia. A
similar osmoregulatory cost of 20% of the net cost of swimming was reported by
Febry and Lutz (Febry and Lutz,
1987
) for exercise-trained (1
BLs-1 for 3 weeks), SW-adapted hybrid tilapia during
prolonged swimming (approximately 2.5 BLs-1). If we accept
these estimates as reasonable for chinook salmon, then it would appear that
the 50% higher
Omax in trained
fish would be more than adequate for partially defending plasma osmolality.
Consequently, it is likely that functions in addition to osmoregulation also
benefited from the training-induced increase in
Omax. Other
possibilities should include protein synthesis and digestion because
exercise-trained chinook salmon can maintain their growth rate despite a
higher energy expenditure (Thorarensen et al.,
1993
; present study). It is
also possible that exercise-trained fish had better stamina and could recover
from exercise faster because there was less of an oxygen debt, but further
experiments would be needed to test these ideas.
Throughout the discussion we have assumed that exercise training was the sole contributor to the observed differences in the trained and control fish. However, this may not be the case. The trained fish were captured by dipnet every other day and this in itself could have contributed to the observed responses. Repeated stress (i.e. the struggling in the dipnet) could have had an additional training effect on the cardiorespiratory system. Similarly, the repeated stress may have desensitized the fish in some way that they were able to perform better in the swim test. Alternatively, the training regime may have reduced the stress response associated with the swim test. Gonzales and MacDonald (Gonzales and MacDonald, 1992) examined the potential effect of acute stress on the osmo-respiratory compromise in FW rainbow trout by injecting adrenaline. They found a short-lived (60 min) but dramatic increase in sodium loss without any change in oxygen uptake, such that one sodium was lost at the gills for every 0.9 oxygen molecules taken up, i.e. a tenfold change compared to resting fish. In the same study, rainbow trout were also shown to be able to physiological adjust to these acute effects on gill ion permeability. For example, after approx. 3 h of continuous swimming at 85% Ucrit and 2-6 h after exhaustive exercise, sodium losses were reduced relative to oxygen uptake. Unfortunately the present data cannot be used to resolve the concern about the role stress may have played in the chronic training effects, but future experiments in which stress hormones are measured might be useful in this respect.
To conclude, our observations on training effects suggest that it is
perhaps time to present a more integrated perspective of the potential
benefits of exercise training to fish. Foremost, an intense and chronic
exercise training regimen was needed to elicit a 50% improvement in
Omax. While this
in itself is not large, the resultant benefits to critical swimming speed and
arterial oxygen transport were smaller still. Direct benefits to
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