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First published online November 28, 2008
Journal of Experimental Biology 211, 3915-3926 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019281
The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka)
Department of Zoology, University of British Columbia, 2357 Main Mall, Vancouver, BC, Canada, V6T 1Z4
* Author for correspondence (e-mail: mfsteinhausen{at}bi.ku.dk)
Accepted 29 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2), cardiac
output (
) and the blood oxygen status
of arterial and venous blood, we were able to determine where in the oxygen
cascade a limitation appeared when fish stopped sustained swimming as
temperature increased. High temperature fatigue of swimming sockeye salmon was
not a result of a failure of either oxygen delivery to the gills or oxygen
diffusion at the gills because oxygen partial pressure
(PO2) and oxygen content
(CO2) in arterial blood did not decrease with
increasing temperature, as would be predicted for such limitations. Instead,
arterial oxygen delivery (TaO2) was initially
hampered due to a failure to adequately increase
with increasing temperature.
Subsequently, lactate appeared in the blood and venous
PO2 remained constant.
Key words: Pacific salmon, cardiac output, heart rate, oxygen consumption, respiration, temperature
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Neill and Bryan, 1991;
Claireaux and Lagardere, 1999;
Claireaux et al., 2000;
Lee et al., 2003;
Lefrancois and Claireaux,
2003). This limitation has been suggested to lead to the use of
anaerobic metabolism, exhaustion, a restriction of whole-animal tolerance to
temperature extremes and even mortality
(Pörtner, 2002;
Pörtner and Knust, 2007).
Aerobic scope, which is defined as the difference between routine and maximal
metabolic rates (Fry, 1971;
Priede, 1977), is often used
to estimate the maximum energy available for activity and assess the impact of
temperature on energy allocation. Aerobic scope peaks at an optimum
temperature (Topt) but decreases with increasing
temperature until it becomes minimal at the critical temperature
(Tcrit) when anaerobic metabolism takes over.
Tcrit arises in part because routine oxygen demand
continues to increase above Topt and in part because
maximum oxygen delivery declines abruptly above Topt.
The temperature dependence of aerobic scope has been successfully applied
to the upriver spawning migration performed by sockeye salmon in the Fraser
River, British Columbia, Canada, which can be exceptionally energy demanding
because of the long migration distance (up to 1000 km) and major hydraulic
challenges (e.g. Hell's Gate). Topt for a given stock of
sockeye salmon has been demonstrated to be similar to the river temperature
encountered during migration (Lee et al.,
2003), suggesting that the physiology of adult spawning salmon may
be optimised to the environmental temperature conditions so that the next
generation of salmon is secured. Correspondingly, when river temperature has
been higher than normal and exceeds Topt, high fish
mortality has been observed in the river
(Farrell et al., 2008). The
temperature dependence of aerobic scope is also being used as a tool to assess
potential impacts of global climate change on fishes
(Pörtner and Knust, 2007;
Wang and Overgaard, 2007;
Farrell et al., 2008).
Despite these broad applications of aerobic scope, the exact mechanism
leading to the decline in maximum aerobic scope above Topt
remains unresolved. Potential mechanisms (gill-related, cardiac-related and
muscle-related limitations) have received theoretical consideration elsewhere
(Brett, 1971;
Taylor et al., 1997;
Farrell, 1997;
Farrell, 2002;
Pörtner, 2002) but
evidence supporting any one of these explanations is sparse and incomplete
[see summary by Farrell (Farrell,
2007a)]. Considerable evidence points to a cardiac-related
limitation, largely because of the similarity of the Topt
values for swimming performance, maximum
O2 and maximum
in salmonids
(Brett, 1971;
Farrell, 1997). However,
Farrell noted the need to further examine whether or not an oxygen diffusion
limitation exists at the gill at temperatures above Topt
(Farrell, 2007a;
Farrell, 2007b). A key
observation in this regard is the demonstration that acute increases in water
temperature decreased both arterial and venous blood oxygen content
(CO2) in resting rainbow trout
(Oncorhynchus mykiss Linnaeus)
(Heath and Hughes, 1973). In
addition, Taylor and colleagues suggested that an oxygen diffusion limitation
at skeletal muscle in swimming fish was important
(Taylor et al., 1997).
In view of this uncertainty, the present study greatly extended on the
earlier study by Heath and Hughes (Heath
and Hughes, 1973) by undertaking simultaneous measurements of
O2,
and oxygen status in arterial and
venous blood of resting and exercising adult sockeye salmon (Oncorhynchus
nerka Walbaum) subjected to an acute increase in water temperature. Given
the excellent swimming ability of sockeye salmon, we reasoned that any
limitation in oxygen delivery during the temperature increase would be better
revealed when fish were swimming near their maximum aerobic capacity rather
than while resting. Consequently, for the exercise component of the study,
salmon were swum continuously at a speed where
O2 was
approaching its maximum [around 75% of their critical swimming speed
(Ucrit) (Brett,
1971; Burgetz et al.,
1998; Lee et al.,
2003)] while temperature was increased. Thus, as temperature
increased at a constant swimming speed, we expected
O2 to increase
only due to temperature-related effects until fish could no longer support
swimming at elevated temperature. We predicted that if there was either a
limitation in oxygen delivery to the gills or an oxygen diffusion limitation
at the gills, then we would observe a decrease in arterial
PO2 when salmon stopped swimming at elevated
temperature. By contrast, if cardiac limitation appeared at elevated
temperature, this would be manifest as a failure to increase
with increasing temperature whereas
an oxygen diffusion limitation to skeletal muscles would be manifest as a
constant venous PO2.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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, temperature=12.5°C) near the mouth
of the Fraser River, BC, Canada. The fish were held in the livehold of the
vessel for a couple of hours while being transferred to and unloaded at the
Centre for Aquaculture and Environmental Research (CAER), West Vancouver, BC,
Canada. Prior to being placed in the holding tank each fish was identified
with a cinch tag, and a scale and a DNA-clip (0.5 g) from the adipose fin were
taken for stock identification. The stock origin of the fish was determined by
DNA and scale analyses (Beacham et al.,
1995; Beacham et al.,
2004). Only fish identified as being from the Lower Adams River
stock complex were used for the present experiments. Salmon were initially
held in a 12,000 l holding tank supplied with full strength seawater at a
temperature of 12.5°C. On the afternoon of the 30th August, the
salinity of the water was decreased over a 4 h period to iso-osmotic
(salinity
9, temperature=13.5°C) by mixing freshwater and
seawater supplies, and the following day the holding tank was switched to pure
freshwater. Freshwater temperature in the holding tank was initially
14.5°C and declined seasonally during the experimental period to
12.0°C by October when the experiments were completed. These changes in
salinity and temperature simulated those experienced by sockeye salmon when
they enter the Fraser River for their spawning migration. In general, one
resting and one exercising fish were tested each day. Therefore, individual
fish were held in freshwater for a minimum of two days and up to a maximum of
28 days before experimentation. All experimental procedures were approved by
the Animal Care Committee of the University of British Columbia in accordance
with the Canadian Council on Animal Care.
Surgical procedures for cardiorespiratory measurements
Each fish was prepared so that arterial and venous blood could be routinely
sampled from in-dwelling cannulae without disturbing the fish and
could be monitored continuously with
a flow probe. For surgery, the fish was first anaesthetised with MS-222 in
buffered freshwater (75 mg l–1 NaHCO3+75 mg
l–1 MS-222, Sigma-Aldrich, St Louis, MO, USA) until opercular
movements ceased. Body mass and length were measured and the fish was placed
ventral side up on water-soaked foam on a surgery table. During surgery, the
gills were irrigated with aerated, chilled water containing a lower dose of
anaesthetic (50 mg l–1 NaHCO3+50 mg
l–1 MS-222, Sigma-Aldrich). To sample arterial blood, a PE-50
cannula filled with a 0.9% saline solution containing heparin (150 i.u.
ml–1) was inserted into the dorsal aorta using an internal
trochar. The cannula was anchored in place at the roof of the mouth using a
3-0 silk suture and exteriorized via a hole in the snout
(Soivio et al., 1973). To
measure , the ventral aorta was
exposed with a 0.5 cm incision on the right side of the isthmus and dissected
free (Steffensen and Farrell,
1998). A Transonic transit-time blood flow probe (3 mm SB,
Transonic systems, Ithaca, NY, USA) was positioned around the ventral aorta,
proximal to the bulbus arteriosus, for measurements of absolute blood flow.
Great care was taken during this procedure to leave the pericardium intact and
avoid damage to the coronary artery. To sample venous blood, a PE-50 cannula
filled with the heparinised saline was inserted into the ductus of Cuvier,
which was carefully exposed and dissected free with an incision between the
cleithrum and the fourth branchial arch
(Farrell and Clutterham,
2003). A small portion of the vessel was lifted and secured with a
vascular clamp and subsequently secured with a 4-0 suture, allowing the vessel
to be gently lifted during the cannulation procedure. A small nick was made in
the lifted vessel and a PE-50 cannula, with 2–3 side-holes and a bubble
1.5 cm from the tip was inserted towards the heart
(Sandblom et al., 2006). A 4-0
suture was used to close the vessel wall around the catheter leaving the
bubble on the luminal side of the vessel. The leads and cannulae were secured
together, sutured onto the body wall with multiple sutures and led off the
leading edge of the dorsal fin. The entire surgical procedure took
approximately 1 h. After being placed in a Brett-type swim tunnel, the fish
recovered from anaesthesia extremely quickly (30–60 s), as
indicated by their ability to maintain an upright position in the water
current and ventilate at a regular frequency. After the first hour of
recovery, the water temperature was ramped up from the holding tank
temperature (12.0–14.5°C) to the experimental starting temperature
of 15°C at a rate of 1°C h–1. This experimental
temperature was expected to be very close to Topt for
aerobic scope based on previous studies with sockeye salmon
(Brett, 1971;
Lee et al., 2003). Each fish
recovered overnight (10–12 h) in a swim tunnel at a temperature of
15°C with the water velocity set at a low flow rate of about 0.20 m
s–1 [approximately 0.35 body lengths s–1
(BL s–1)]. At this modest water speed, salmon faced
into the water flow and maintained station without any tail beats.
Experimental protocols
The two experimental protocols were essentially identical in terms of the
protocol to acutely increase temperature above Topt but
were performed on either resting or exercising fish. Both protocols began with
measurements of routine
O2 and
over a 30–45 min period. At the
end of this recording period, 0.7 ml of blood was withdrawn from the arterial
and venous cannulae using heparinised syringes and the collected blood volume
was replaced with 0.9% NaCl. The protocol for resting fish (N=18
fish) involved increasing the water temperature at a rate of 2°C
h–1 to each of the following test temperatures: 17, 19, 21,
23 and 24°C. The cardiorespiratory measurements were repeated in
duplicate, starting immediately after a stable temperature was reached. All
resting fish completed the 24°C temperature exposure protocol, after which
water temperature was decreased to 15°C over a 45 min period and the
recovery of cardiorespiratory status was evaluated by repeating measurements
after approximately 1 h.
The second group of fish (swimming fish; N=15) were first required
to swim at a steady-state before they were tested with the same acute
temperature protocol. Thus, after taking routine cardiorespiratory
measurements, the water velocity in the swim tunnel was increased by 0.1 m
s–1 every 2 min until a final velocity of 0.85 m
s–1 (1.35 BL s–1) was reached.
Preliminary experiments (data not shown) had shown that at this temperature,
the fish were swimming at approximately 75% of Ucrit and
they could sustain this speed in excess of 4 h. By having the fish swimming at
a fixed swimming speed (1.35 BL s–1), we could use
temperature as a continuous factor in a repeated-measures statistical design
for analysis of variance (RM ANOVA). The fish were maintained at the sustained
swimming speed for 30 min to allow the physiological variables to reach a
steady state before measuring the cardiorespiratory status of swimming fish at
15°C. The expectation was that 75% Ucrit placed these
fish near to their maximum aerobic scope
(Lee et al., 2003) and that,
with the subsequent increase in water temperature, the associated increase in
tissue oxygen demand and the decrease in aerobic scope at a temperature above
Topt would cause the fish to eventually quit swimming. All
fish swam at 19°C but only three fish swam at 24°C, the remainder
quitting at intermediate water temperatures
(Fig. 1). Regardless, of the
final temperature, water flow was reduced to 0.2 m s–1 when
the fish quit swimming and the water temperature was reduced to 15°C. The
recovery of cardiorespiratory status was evaluated by repeating measurements
after approximately 1 h, as with the resting fish.
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;
Farrell et al., 2003). A
shocking grid at the rear end of the tunnels was used to provide a mild
electrical stimulation (2–10 V) to prevent the fish from resting on the
grid during swimming. Water velocity was measured with an anemometer (Valeport
Marine Scientific, Dartmouth, UK) and calibrated against the motor frequency
for each tunnel (Farrell et al.,
2003). Temperature was controlled by a custom-designed heating
system. A 9 kW titanium heating element was installed directly into the swim
tunnel vessel to provide controlled increases in water temperature (up to
12°C above ambient). During a measuring period, the water temperature
never fluctuated by more than 0.5°C.
O2 and measurements
O2 was
measured by closing the water inflow and outflow from the swim tunnel. The
decrease in water oxygen content was measured with an Oxyguard probe (Mark IV,
Point Four Systems, Richmond, Canada) that measured oxygen levels with a
precision of 3 mol l–1. The oxygen probe was placed in a
small chamber (0.3 l) outside the swim tunnel and a pump (Eheim Universal
1046, Loligosystems, Tjele, Denmark) placed in the loop created a flow-through
of water (5 l min–1) over the probe. The probe reading was
digitised via a Windaq box (Dataq instruments, Akron, ON, USA) and
data were saved at a frequency of 0.2 Hz using software programmed in Labview
6.0 (National Instruments, Austin, TX, USA). The duration of the measuring
period (ranging from 3–45 min) was determined by a suitable decrease in
oxygen content (
10 mol l–1) and was dependent on the size
of the fish and activity level, i.e. routine
O2 measurements
at the coldest temperature took the longest time, while those for the swimming
fish were the shortest. The decline in water oxygen content over time resulted
in a linear regression with r2 values of 0.95.
O2 (µmol
min–1 kg–1) was calculated as:
O2 =
[O2]vMb–1t–1,
where [O2] is measured in µmol l–1,
v is the volume of the swim tunnel minus the fish volume in litres,
Mb is body mass in kilograms and t is time
measured in minutes.
was monitored simultaneously
during O2
measurements. The flowprobe was connected to a Transonic flowmeter (Model
T206, Transonic Systems, Ithaca, New York, USA). Blood flow data was sampled
at 200 Hz using a Biopac module running Acknowledge 3.8.2, (Biopac Systems,
Santa Barbara, CA, USA). (ml
min–1 kg–1) was calculated as a mean of
three periods of 10–20 s when a stable cardiac rhythm was present. Heart
rate (fH; beats min–1) was calculated
from the intervals between systolic peaks in the flow trace and cardiac stroke
volume (Vs; ml beat–1
kg–1) was calculated as Vs =
fH–1.
As the swimming velocity was never increased until fish reached their
maximum cardiorespiratory performance at a fatigue velocity, aerobic scope and
cardiac scope were never measured directly in any fish. However, because fish
were swimming near their maximum
O2 at 75%
Ucrit, we therefore expected that ultimately the acute
increase in temperature would create a situation where aerobic scope was
reached, either because routine
O2 had
progressively increased, maximum
O2 had declined
above Topt, or, more likely, some combination of the two.
At this juncture, a further increase in water temperature would cause fish
either to quit swimming aerobically or to compliment the aerobic effort with
anaerobic swimming. To visualise such effects and to properly account for the
temperature effect on routine metabolism, we calculated the difference (termed
range) between the routine and swimming values for
O2,
and fH. Because these
values were derived from the mean values from two different groups of fish
(resting and swimming) at each temperature, no statistical inferences can be
made from these data. To simplify this presentation, range is presented as a
percentage of the highest value obtained which was at 17°C for
fH and 19°C for
O2 and
.
Blood analyses
Blood samples were placed on ice and immediately analysed for
PO2, O2 content
(CO2), pH, haemoglobin concentration (Hb) and
haematocrit (Hct). The remaining blood was spun down and the plasma was frozen
in liquid nitrogen and stored at –80°C for subsequent analysis.
Blood PO2 was measured with a Radiometer
PO2 electrode (E101, Loligosystems, Tjele,
Denmark), thermostatted in a D616 cell at the respirometer temperature, and
displayed on a Radiometer PHM 71 acid–base analyzer. The electrode was
calibrated with air-saturated water several times daily and in accordance with
the experimental temperature changes from 15–24°C.
CO2 of whole blood was measured according to
Tucker (Tucker, 1967).
Arteriovenous O2 delivery
(A
O2) was
calculated as the difference between arterial and venous
CO2 using data only from fish where both blood
samples were successfully drawn and analysed. Arterial O2 delivery
(TaO2) was calculated as the product of
and arterial
CO2. Blood pH was measured from 0.2 ml of
blood, which was injected into a custom designed plastic chamber housing a
snugly fit pH probe (Symphony 14002-764, VWR, PA, USA). The blood was
thermostatted to the experimental temperature and whole blood pH values were
read on a handheld pH meter (Symphony SP301, VWR, PA, USA). Haemoglobin
concentration was determined spectrophotometrically on 10 µl of blood using
a Randox total haemoglobin assay kit (HG980, Randox Laboratories, Antrim, UK).
Plasma lactate, potassium and cortisol concentrations were measured on samples
that were thawed immediately before use and vortexed for 30 s before use in
accordance with the methods fully described by Farrell and colleagues
(Farrell et al., 2001).
Lactate was measured in duplicates using an YSI 2300 lactate/glucose analyzer
(Yellow Springs Instruments, OH, USA) that was automatically calibrated every
five measurements to a precision of 0.2 mmol l–1. Potassium
was measured in duplicate on a flame photometer (Cole Parmer model 2655-00,
Vernon Hills, IL, USA) after dilution of the plasma (deionized water 1:200).
The flame photometer was calibrated prior to use with a four-point calibration
and standards were checked every 10 samples. Plasma cortisol concentrations
were measured in duplicates using an ELISA kit (Neogen, Lexington, KY, USA).
Only arterial values for Hb, lactate, potassium and cortisol are presented
because we did not expect large differences with the venous values and there
were lower numbers of successful venous samples.
Statistics
Given that no significant differences were found between male and female
fish, the data were pooled. All data were analysed using a two-way (swimming
vs resting or arterial vs venous) RM (temperature) ANOVA and
Tukeys' test was used for all pairwise comparisons. In some cases the ANOVA
design was disconnected, which did not permit a two-way test and so the data
were analysed using a one-way RM ANOVA followed by a Student's t-test
to separately compare either swimming vs resting fish or arterial
vs venous blood samples. A Spearman correlation test was used to
analyse the correlation between rank performance (based on different
cardiorespiratory parameters) and the temperature at which fish quit swimming.
All values are means ± s.e.m. and statistical difference was assigned
for a P-value<0.05.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Fish swam steadily and continuously at water temperatures between 15°C and 19°C, as would be expected for sustained swimming near to maximum aerobic performance. However, at water temperatures of 19°C and above, the swimming mode included an increasing contribution of burst and coast activity, which is indicative of a switch to anaerobically powered swimming using white muscle fibres.
All fish completed the swimming protocol at 19°C. However, above this temperature, the number of fish able to maintain station at the imposed swimming speed declined with increasing temperature (Fig. 1) and only three out of 15 fish completed the swimming protocol at 24°C. The temperature for a 50% failure to swimming was interpolated from Fig. 1 as 23.5°C. Therefore, increasing temperature induced a change in swimming behaviour and caused some fish to quit swimming, as predicted. These behavioural changes occurred at and above 19°C, and were associated with important physiological changes (as shown below). Nevertheless, these changes did not prevent the fish from making a rapid recovery when returned to 15°C (as shown below).
Because of these behaviours, the physiological data presented in subsequent
figures necessarily represent only the fish that swam at a given temperature,
i.e. a decreasing N value above 19°C. Implicit for such
presentations is that only the temperature-tolerant or best performers are
represented for the highest temperature, creating a potential bias. Therefore,
the cardiorespiratory variables at fatigue, regardless of the temperature at
which fatigue occurred, are summarised for all fish in
Table 1. These values are
representative of the average physiological state at fatigue following an
acute temperature challenge. Given the fact that Ucrit
varies among individuals, a further difficulty with a fixed speed swimming
protocol and progressive increases in temperature is distinguishing between
temperature tolerance and best performers. Therefore, to shed light on whether
fish quit swimming because of the increase in temperature per se or
because the imposed swimming speed was closer to their real
Ucrit, we examined for relationships between the
temperature at which a fish quit and the ranking of various key
cardiorespiratory variables (routine
O2, routine
,
O2 swimming at
15°C and swimming at 15°C). No
significant relationships were found.
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Oxygen uptake
In resting sockeye salmon, routine
O2 increased
significantly with each temperature increment
(Fig. 2A), resulting in a
3.2-fold increase between 15°C and 24°C (an overall
10 value of 3.6). The
10 values between each of the test
temperatures varied from the lowest
10 value of 3.2 between 19°C and
21°C to the highest 10 value of
4.2 between 17°C and 19°C. When fish were returned to a temperature of
15°C for 1 h, routine
O2 was largely
restored to the initial routine
O2 value but
remained significantly elevated by 29%
(Fig. 2A).
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O2 at
15°C for the group of swimming fish prior to swimming was identical to
that measured at 15°C for the resting fish group
(Fig. 2A). Swimming at
approximately 75% of Ucrit at 15°C significantly
increased O2,
such that active
O2 was 6.5-times
higher than routine
O2
(Fig. 2A;
Table 1). Increasing water
temperature initially increased active
O2 significantly
(Fig. 2A). However, active
O2 was not
significantly different between 19°C and 24°C, and active
O2 at 24°C
was no different to that measured at 17°C
(Fig. 2A). Thus, active
O2 reached a
maximum and showed indications of a decline at 24°C, unlike the continuous
increase in O2
in the resting fish group.
When fish stopped swimming and the temperature was returned to 15°C,
O2 decreased
significantly but remained significantly elevated by 65% above the initial
routine O2 value
at 15°C (Fig. 2A;
Table 1).
Across all temperatures, the increase in routine
O2 was not
matched with the change in active
O2, as shown by
the range for O2
(Fig. 3). The range for
O2 was maximal
at 19°C (362.5 µmol min–1 kg–1). This
means that range for
O2 increased
modestly with an increase in temperature from 15°C to 19°C, was
maintained at 21°C and then declined at temperatures of 23°C and
24°C.
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increased
significantly with temperature (Fig.
2B), increasing by 70% between 15°C and 24°C (an overall
10 value of 1.7). The values between
each of the test temperatures varied from the lowest
10 value of 1.1 between 23°C and
24°C to the highest 10 value of
2.2 between 19°C and 21°C. When fish were returned to a temperature of
15°C for 1 h, routine was almost restored
to the initial value but remained
significantly elevated by 17% (Fig.
2B).
While the temperature-induced increase in routine
paralleled that in
O2
(Fig. 2), there was an
important difference. Routine reached a
plateau at 23°C (Fig. 2B)
whereas routine
O2 did not
(Fig. 2A). Notably, the
temperature-induced increase in routine was
brought about through fH increasing from 64 beats
min–1 to over 100 beats min–1
(Fig. 4A), and little change in
VS from the routine value of 0.38 ml
beat–1 kg–1
(Fig. 4B). Routine
fH was almost restored during recovery at 15°C, but
remained significantly 16% higher during recovery
(Fig. 4A).
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at 15°C for fish resting before
swimming was identical to that measured in the resting fish at 15°C.
Swimming at 15°C increased by 2.3-times
(Table 1;
Fig. 2B). Active
increased significantly with the initial
temperature increase (Fig. 2B)
but did not increase subsequently between 17°C and 24°C
(Fig. 2B). When fish stopped
swimming and recovered at 15°C for 1 h,
decreased significantly but remained significantly elevated by 33% compared
with the initial routine value
(Fig. 2B;
Table 1).
Across all temperatures, the increase in routine
was not matched with the change in active
, as shown by the range for
(Fig.
3). The range for was maximal at
19°C. This means that the range for
increased modestly with an increase in temperature from 15°C to 19°C
was maintained up to 21°C and declined at temperatures of 23°C and
24°C.
Prior to swimming at 15°C, routine fH and
Vs (Fig. 4)
were identical to those measured at 15°C for the resting fish group. Fish
swimming at 15°C elevated fH by 20%
(Fig. 4A) and
Vs by 80% (Fig.
4B). The temperature-induced increase in active
came about solely though increased
fH (Fig.
4A), as in resting fish. Although there was no increase in
Vs with temperature, Vs remained
significantly elevated above that measured in resting fish
(Fig. 4B). Noticeably,
fH did not increase significantly as temperature was
increased above 19°C and, as a result, fH for swimming
and resting fish converged at just over 100 beats min–1 when
water temperature reached 24°C. Consequently, active
fH was significantly higher than resting
fH at all temperatures except 24°C
(Fig. 4A). Thus, the range for
fH was greatest at 17°C but declined to near zero at
24°C (Fig. 3). In addition,
cardiac rhythm became more variable at high temperatures (data not shown),
which may have contributed to the increased variability around the mean values
for fH at 23 and 24°C
(Fig. 4). While
Vs was fully restored after a 1 h at 15°C,
fH remained significantly elevated by 25% compared with
the resting fish (Fig. 4A).
Hb, Hct, pH, lactate, potassium and cortisol
Hb and Hct (Table 1) were
unchanged during the acute temperature change, indicating that anaemia did not
develop despite repeated blood sampling.
In resting fish, arterial and venous blood pH values were not significantly different at any temperature (Fig. 5A). However, at 24°C venous blood pH was significantly reduced compared with the routine values at 15°C and this corresponded with a significant increase in the plasma lactate concentration (Table 1; Fig. 6A). Plasma cortisol (Fig. 6B), but not plasma potassium (Fig. 6C), increased significantly with temperature in resting fish and all these variables were restored after a 1 h recovery at 15°C.
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Arterial and venous blood 
O2 and CO2 values
In resting fish, both venous and arterial
PO2 increased significantly with temperature
(Fig. 7A). However, there were
no corresponding increases in the CO2 of
arterial or venous blood (Fig.
8A), probably because of a right-shift in the HbO2
dissociation curve with increasing temperature. Routine
PO2 values were restored after a 1 h recovery
period at 15°C (Fig.
7A).
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|
Venous and arterial routine PO2 values for swimming group resting at 15°C were identical to those measured at 15°C for the resting fish group (Fig. 7). Swimming at 15°C induced significant decreases in venous PO2 (Table 1; Fig. 7B) and venous CO2 (Table 1; Fig. 8B), the latter indicating an increased extraction of oxygen from the blood by the skeletal muscles. Swimming at 15°C also induced significant decreases in arterial PO2 (Table 1; Fig. 7B) and arterial CO2 (Table 1; Fig. 8B).
Increasing temperature during swimming had no significant effect on either venous PO2 (Fig. 7B) or venous CO2 (Fig. 8B). Venous CO2 but not venous PO2 was reduced significantly at fatigue (Table 1). Swimming at 19°C restored routine arterial PO2 and CO2 to the routine levels measured at 15°C and arterial PO2 was then maintained at all temperatures above 19°C (Fig. 7B; Fig. 8B). Recovery for 1 h at 15°C fully restored routine blood O2 status for the swimming group of fish (Fig. 7B, Fig. 8B).
Oxygen delivery across the gills and to tissues
Despite the inability of active
O2 and active
to increase further as temperature was acutely
increased above 19°C, arterial PO2 never
decreased with increasing temperature in either resting or swimming sockeye
salmon. These results support the conclusion that neither the delivery of
water to the gills nor the diffusion of oxygen from water to the blood was a
limiting factor.
TaO2 increased significantly when fish began
to swim and this was a result of increased
(Fig. 9A). However, increasing
temperature during swimming did not increase
TaO2 any further and at fatigue
TaO2 was no higher than for fish swimming at
15°C (Table 1).
|
O2 was
significantly higher for fish at fatigue compared with fish swimming at
15°C (Table 1), indicating
that the acute increase in water temperature at a constant swimming speed
caused an increased extraction of oxygen from the blood by the tissues. This
increase in AO2
at fatigue did not reach statistical significance when
AO2 was plotted
against temperature (Fig. 9B)
but AO2 tended
to increase with temperature when active had
already reached a maximum.
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
O2,
and blood oxygen status simultaneously. The
experiments were explicitly designed to swim fish above their
Topt and increase temperature to elicit the collapse in
aerobic scope that has been demonstrated in previous studies
(Lee et al., 2003;
Farrell et al., 2008).
Although we could not directly measure aerobic scope with the present
experimental design, it was clear from the plateau in
O2 for swimming
fish above 19°C, the increased reliance on glycolytic swimming and the
fact that most fish quit their sustained swimming effort at temperatures below
24°C (without any relationship to their rank order of cardiorespiratory
performance) that aerobic scope was clearly compromised at temperatures above
19°C. Regardless, the primary purpose of the present study was not to
define either this decline or Topt but to provide insights
into the underlying mechanisms for cardiorespiratory failure at high
temperature.
At the outset we predicted that a decrease in arterial
PO2 with increasing temperature would indicate
that there was either an oxygen diffusion limitation at the gills or a limit
in oxygen delivery to the gills. This result was not obtained, as neither
arterial PO2 nor arterial
CO2 decreased in response to acute temperature
increases for either resting or swimming sockeye salmon. By contrast, a
cardiac limitation was manifest as revealed by the failure of swimming fish to
progressively increase with increasing
temperature, with fH apparently reaching a maximum and
TaO2 not being increased at fatigue. Given this
temperature limitation on TaO2, swimming fish
were able to increase
AO2 at fatigue
(when temperature was above 19°C). However, this increase in
AO2 came about
because of a decrease in venous CO2 and with a
constant venous PO2. The most parsimonious
explanation for this result is that the temperature-induced right-shift in the
HbO2 dissociation curve permitted greater oxygen unloading from the
haemoglobin. This then suggests that either following or associated with
temperature limitation on TaO2, there is a
limitation on oxygen diffusion into locomotory skeletal muscle, otherwise
venous PO2 would have decreased as tissue
oxygen demand increased with increasing temperature.
Fish performance during an acute temperature increase
Routine O2
increased continuously with temperature, apparently following a simple
10 effect up to 24°C. While all
resting fish tolerated 24°C, the increased exploratory behaviour when the
temperature reached 19°C and the increases in plasma lactate and cortisol
concentrations above 19°C, which probably reflect an increased reliance on
anaerobic metabolism, confound this interpretation somewhat. At temperatures
above 19°C, fish also changed their swimming gait, perhaps because active
and TaO2 had
reached maximum values. Thus, for this particular stock of sockeye salmon, a
temperature of 19°C appears to be a transition temperature for behaviour
and physiology during an acute increase in water temperature. Only 20% of fish
were able to swim at 75% Ucrit when water temperature
was raised to 24°C.
In the present study, sockeye salmon swam at an estimated 75% of
Ucrit at 15°C and their
O2 was
approximately 70% of maximum
O2. In addition,
70–75% of Ucrit is generally considered to be near
the swimming speed at which the onset of anaerobic metabolism begins (Burggetz
et al., 1998; Holk and Lykkeboe,
1998; Lee et al.,
2003). While we cannot be certain that all fish were close to
their maximum
O2, we can be
certain that the active
O2 and
values measured here are among the highest
literature values for salmonids (Farrell,
2002; Lee et al.,
2003; Wagner et al.,
2005).
We cannot be absolutely certain that the individual variability in
Ucrit coupled with the fixed swimming speed of 1.35
BL s–1 resulted in fish swimming at different
percentages of Ucrit and this factor, rather than
temperature per se, contributed to fatigue (i.e. experimental
duration and not increased temperature was the principal cause of fatigue). We
suspect that this was not the case for a number of reasons. Foremost, these
fish were captured before they entered the Fraser River and started an arduous
upstream migration. Consequently, our experimental fish were likely
well-provisioned and well-prepared for a sustained swim against a high
velocity river system at a rate of 20–50 km per day for several weeks.
Therefore, beyond the imposed temperature challenge, several hours in a swim
tunnel was probably not an excessive challenge, as evidenced by the rapid rate
of recovery at 15°C post-exercise. Indeed, preliminary experiments showed
that these fish sustained the imposed level of swimming performance for >4
h at 15°C without any increase in plasma lactate levels. Furthermore, had
fatigue been solely a result of the individual variation in swimming
performance, we might have expected the poorer swimming fish (e.g. those with
a lower maximum
O2 and
values) to fatigue at the lowest temperatures.
However, this was not the case when we examined for relationships in rank
performance and the fatigue temperature. A critical physiological observation
was that, either at 24°C for resting fish or at the fatigue temperature
for swimming fish, these sockeye salmon had exhausted their scope for
increasing fH.
Elevating temperature above Topt was expected to
increase the reliance on anaerobic metabolism (see Introduction). Similarly
when sockeye salmon approach Ucrit, they change swimming
gait, activate glycolytic white muscles, produce lactate and decrease blood pH
(Brauner et al., 2000).
Increases in plasma cortisol are also recognised as a sensitive indicator of
thermal stress in several fish species
(Gamperl et al., 1994;
Mommsen et al., 1999). Here,
we observed most of these changes, with plasma lactate, cortisol and
K+ concentrations all increasing significantly at fatigue compared
with swimming values at 15°C. The high plasma K+ concentration
reported in a number of fish studies
(Nielsen and Lykkeboe, 1992;
Nielsen et al., 1994;
Holk and Lykkeboe, 1998) is
due to the loss of K+ from working muscles. High plasma
K+ levels may result in inexcitability of the muscle cells in
general (i.e. skeletal and cardiac) and may have contributed to the fatigue of
sockeye salmon at high temperatures.
Aerobic scope has been previously measured in temperature acclimation
studies and shown to be 280 mol min–1 kg–1
at the Topt of 15.0°C for the Weaver Creek and 336 mol
min–1 kg–1 at 17.5°C for the Gates Creek
stocks of sockeye salmon (Lee et al.,
2003). Brett reported an aerobic scope of 400 mol
min–1 kg–1 at a Topt of
15°C for an undetermined stock of Fraser River sockeye salmon
(Brett, 1971). Here, we used
ranges to illustrate the temperature effects on the
O2,
and fH. The various
aerobic scope values measured among different studies and stocks of sockeye
salmon compare favourably with the maximum
O2 range
measured here as 362 mol min–1 kg–1 for the
Lower Adams River sockeye at 19°C. Thus, either the Lower Adams River
sockeye have a considerably higher aerobic scope than other stocks or our
experiments were extremely close to the revealing of a true maximum aerobic
scope.
Tcrit values have been estimated as 20.4°C for
Weaver Creek and 24.4°C for Gates Creek sockeye salmon, respectively
(Farrell et al., 2008), by
extrapolation of the data on aerobic scope at acclimated temperatures
(Lee et al., 2003). Again, we
did not directly measure either Topt or
Tcrit but only 20% fish tolerated swimming at 24°C,
and if we assume that fish had zero aerobic scope at the temperature they quit
swimming, a polynomial for the
O2 range
(Fig. 3) yields an intercept of
25°C, a temperature not unlike the Tcrit for Gates
Creek sockeye salmon.
The absence of a limitation in gill oxygen uptake
As oxygen saturation of water decreases by 2%
°C–1, the availability of oxygen is lower in warm
compared with cold water (Dejours,
1975). Increasing temperature also facilitates unloading rather
than loading of oxygen as the HbO2 dissociation curve is shifted
down and to the right with elevated temperature
(Jensen et al., 1998).
Consequently, a limitation on gill oxygen uptake (either delivery of water to
or diffusion of oxygen across the gills) has been suggested to be a
significant factor explaining high temperature fatigue in fish. In support of
this idea, Heath and Hughes measured decreased
CO2 in arterial blood (and venous blood) of
resting rainbow trout (Oncorhynchus mykiss Walbaum) when temperatures
exceeded approximately 22°C (Heath and
Hughes, 1973). By contrast, the present study showed that arterial
CO2 remained constant for resting and swimming,
as well as fatigued sockeye salmon over the entire experimental temperature
range. These results clearly demonstrate that oxygen uptake across the gills
was not limited in the present experiments. In addition, arterial
PO2 for resting fish significantly increased
with increasing temperature and was constant for swimming fish, which clearly
demonstrates that neither water delivery to the gills nor oxygen diffusion
across the gills were limited with acute temperature increases in sockeye
salmon.
Why a difference exists between the present data and those for rainbow
trout is unclear. The difference cannot reside with the fact that the previous
work was only performed on resting rainbow trout, since we obtained similar
results for both resting and swimming sockeye salmon. A possible explanation
may reside with a difference between hatchery and wild fish. For example, the
gills of wild sockeye salmon being better designed for oxygen transfer than
the gills of hatchery-raised rainbow trout. Yet another explanation may rest
with the experimental apparatus used to house fish. Although we do not know
the nature of the aquarium used previously with rainbow trout, restrictive
blackened square boxes were in vogue. In the present study, sockeye salmon
took advantage of the water current in the swim tunnel, perhaps reducing
ventilatory effort. Further studies investigating the role of ventilatory
effort on a fish's ability to fully saturate arterial blood at high
temperature are worth undertaking. Along these lines, a decline of arterial
PO2 in resting adult Chinook salmon (O.
tshawytscha Walbaum) with increasing temperature was related directly to
body size (Clark et al., 2008),
perhaps because larger fish were more constrained than smaller fish and this
limited or increased ventilation effort.
To our knowledge, the increase in arterial
PO2 that we observed with increasing
temperature has not been previously demonstrated in fish but it is not
unexpected given the decreased HbO2 affinity (Bohr-effect)
associated with warm temperatures in fish
(Randall et al., 1997) or even
an increase in the effectiveness of gill oxygen exchange. Arterial
CO2 was unchanged despite the increasing
routine arterial PO2 with temperature,
suggesting that arterial blood was near full oxygen saturation. Physically
dissolved oxygen contributes minimally to the arterial
CO2 as the presence of haemoglobin increases
blood oxygen content many fold (Randall et
al., 1997). Other alterations in the HbO2 dissociation
curve occur during long-term acclimation to high temperatures, such as a
decreased level of organic phosphate in the erythrocyte, increased Hb
concentration and changes in the synthesis of Hb components
(Jensen et al., 1998) but were
unlikely to be a factor in these short temperature exposures.
The release of red blood cells from the spleen can occur quickly during
swimming (Gallaugher and Farrell,
1998) and with a moderate acute temperature increase
(Sandblom and Axelsson, 2007).
While we saw no increase in haemoglobin concentration, it is possible that the
extensive blood sampling masked this effect.
A limitation on maximum cardiac performance at high temperature
The increased
O2 with
temperature was supported initially by increased
and by increased
AO2 near
fatigue. However, in swimming fish TaO2 clearly
reached a maximum, as did active and
fH with increasing temperature. Furthermore, these maxima
corresponded to a temperature when sockeye salmon changed their swimming gait,
increased plasma lactate and then started to fatigue as temperature was
increased further.
The maximum fH observed in the present study (106
min–1) is close to the suggested maximum of 120 beats
min–1 for active fish
(Davie and Farrell, 1991).
Resting and active fH converged above 19°C and were
identical at 24°C. These changes in fH probably
reflect direct temperature effects on the pacemaker even though the onset of
swimming at 15°C increased routine fH by about 25% and
Vs by more than 80%. As a result, active fH
reached a maximum at a lower temperature than routine fH.
While, we know nothing of cardiac control mechanisms under such temperature
situations, these results point to the upper temperature limits for maximum
cardiac pumping ability being, in part, a result of a maximum
fH being reached.
The absence of any increase in Vs during an acute
increase in temperature has been observed previously in resting fish
(Gollock et al., 2006). The
present observations add further intrigue to this observation, because
apparently Vs was fixed at different levels, independent
of fH, for resting and swimming sockeye salmon. The basis
for this response is a matter of speculation because of the multiple factors
that can influence Vs. For example, acidosis inhibits
cardiac contractility (Driedzic and
Gesser, 1994), and so the observed decrease in venous pH with
increasing temperature could have constrained cardiac inotropy during
swimming. In addition to low pH, low venous oxygen and elevated plasma
potassium have negative inotropic effects that could also limit maximum
cardiac pumping capacity (Farrell et al.,
1996; Hanson et al.,
2006). These debilitating effects would be exacerbated if the
protective effect of adrenaline on cardiac tissues was diminished at warm
temperatures, as is the case in rainbow trout
(Farrell et al., 1996;
Hanson and Farrell, 2007).
Furthermore, if increases in fH are inevitable because of
direct temperature effects on pacemaker cells, then cardiac filling time is
progressively reduced and the negative force–frequency relationship
common to many fish hearts (Shiels et al.,
2002) may further constrain on Vs at high
temperature. It can also be speculated that mobilization of blood from the
venous capacitance vasculature is impaired at high temperatures that may
result in a reduced cardiac filling pressure, which limits
Vs (Sandblom and
Axelsson, 2007). While all of these factors could contribute to
greater or lesser extents in high temperature fatigue, central cardiac control
cannot be excluded. We observed considerable cardiorespiratory synchrony at
high temperature (data not shown). Randall reported that efferent bursting
activity recorded from the cardiac vagus of tench (Tinca tinca
Linnaeus) was synchronous with the mouth-opening phase of the respiratory
cycle (Randall, 1966).
Furthermore, recent data show that vagal burst activity can entrain
fH (E. W. Taylor, personal communication), opening the
possibility for reflex control of fH.
Limitations on tissue oxygen extraction
To compensate for the temperature independence of
TaO2 for sockeye salmon swimming above
17°C, AO2
was increased near fatigue. Increased
AO2 is a common
response of salmonids during incremental velocity swimming so that the
increased oxygen demand of locomotory muscles is satisfied
(Stevens and Randall, 1967;
Kiceniuk and Jones, 1977;
Gallaugher et al., 2001;
Brauner et al., 2000), and a
similar plateau in venous PO2 was observed for
swimming rainbow trout just before Ucrit was reached
(Farrell and Clutterham,
2003). Heath and Hughes (Heath
and Hughes, 1973) acutely warmed resting rainbow trout and
observed a constant
AO2 with
increased temperature but this was because arterial and venous
CO2 both decreased in proportion, a response
that was not observed in the present experiments. In itself, the modest 50%
increase in AO2
observed here suggests that oxygen extraction by locomotory muscle can
increase when sockeye salmon exceeded their aerobic threshold at high
temperature and that tissue oxygen delivery does not become diffusion limited.
However, the observed plateau in venous PO2
with increasing temperature in swimming fish seems to argues for such a
diffusion limitation, which would be in accord with the previous proposal for
rainbow trout swimming at high temperature
(Taylor et al., 1997). In
fact, the plateau in venous PO2 in swimming
rainbow trout just before Ucrit has been similarly
interpreted as evidence for a diffusion limitation on tissue oxygen extraction
(Farrell, 2007a). In the
present study, the increase in
AO2 without a
decrease in PO2 probably came about because
increasing temperature causes a right-shift in the HbO2
dissociation curve, i.e. there was greater unloading of oxygen from Hb. We
then speculate that venous PO2 could not
decrease any further due to a diffusion limitation. Even so, other
possibilities besides an oxygen diffusion limitation could explain the present
results, the most likely being that tissue oxygen utilization decreases at
high temperature. A decrease in tissue oxygen utilisation could arise because
either the high temperatures begin to impair cellular function in swimming
fish or the rate of ATP generation by oxidative phosphorylation is simply not
fast enough for the tissue ATP demand and so they switch to a faster rate of
ATP generation through glycolysis, much like the gait transition that
salmonids undertake as they switch from red to white muscle powered locomotion
when they swim faster.
If a diffusion limitation for oxygen extraction does exist in white muscle
during locomotion, it may represent important cardioprotective mechanism
because the venous blood still has to supply oxygen to the ventricle in fish
such as salmon (Davie and Farrell,
1991) and this oxygen supply is thought to be ultimately limited
by the venous PO2
(Farrell, 1987). For swimming
fish, venous PO2 remained between 22 and 28
Torr with increasing temperature. Lower venous
PO2 values of around 10 Torr have been reported
for resting hypoxic fish (Davie and
Farrell, 1991), as well as for rainbow trout swimming moderately
in hypoxic water (Steffensen and Farrell,
1998). A higher myocardial oxygen demand may account for a higher
venous PO2 for sockeye salmon exercising at
high temperature (Farrell,
2007b). Indeed, Farrell and Clutterham
(Farrell and Clutterham, 2003)
found a higher venous PO2 threshold value of 29
Torr for warm-acclimated (13–16°C) than the 15 Torr for
cold-acclimated (6–10°C) swimming rainbow trout. In addition, the
threshold oxygen concentration for the working perfused rainbow trout heart is
greatly increased at high temperature if acidotic and high K+
conditions exist (Hanson et al.,
2006; Hanson and Farrell,
2007).
Recovery of sockeye salmon
Despite experiments lasting many hours, and a swim challenge in one group
of fish, sockeye salmon had largely recovered their cardiorespiratory status
after only 1 h at 15°C.
O2 of resting
fish was only 30% higher and and
fH were only 17% higher than routine values whereas
swimming fish had 66% higher
O2 and 33%
higher and fH values. All
other parameters were restored to the initial routine levels, with only plasma
lactate and cortisol as exceptions. The release of lactate from the exhausted
muscles to the blood does occur over several hours
(Milligan et al., 2000), thus
explaining the elevated lactate concentration after just 1 h recovery. In
addition, salmon recovered while resting and moderate activity keeps plasma
lactate and cortisol levels down (Farrell
et al., 2001; Milligan et al.,
2000).
The type of physiological resilience exhibited here by sockeye salmon is
probably needed while they experience large daily temperature fluctuations of
up to 6°C (Lee et al.,
2003) and up to 10°C over the course of an approximately three
weeks upriver migration (Idler and
Clemens, 1959). The rapid recovery observed here may be related to
a faster metabolic recovery at higher temperatures as shown for other
salmonids after being chased to exhaustion
(Kieffer and Tufts, 1996;
Galloway and Kieffer,
2003).
In summary, we conclude that high temperature fatigue in swimming sockeye salmon is due to a cardiac limitation resulting in insufficient oxygen delivery to working muscles. To compensate, oxygen extraction by skeletal muscle did increase modestly at fatigue but diffusion of oxygen to skeletal muscles was probably restricted. By contrast, oxygen uptake over the gills was not limited and is therefore insignificant in explaining high temperature fatigue of sockeye salmon.
LIST OF ABBREVIATIONS
O2
O2
|
Acknowledgments |
|---|
|
References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
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) sockeye salmon during an acute temperature increase of
2°C h–1. For swimming fish, an initial resting value at
15°C was obtained prior to swimming (
). At the end of the acute
temperature increment, water velocity for the swimming fish was immediately
decreased to the resting level and the temperature was decreased to 15°C
over an hour before a recovery measurement was recorded for both groups. All
values are means ± s.e.m. Different letters indicate significant
differences between temperatures within the same group. An asterisk indicates
a significant difference between resting and swimming fish at a given
temperature.
) from the mean values presented in Figs
