The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks
1 Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6,
Canada
2 Department of Forest Sciences, University of British Columbia, Vancouver,
BC, V6T 1Z4, Canada
3 Department of Zoology, University of British Columbia, Vancouver, BC, V6T
1Z4, Canada
4 Institute for Resources and Environment, University of British Columbia,
Vancouver, BC, V6T 1Z4, Canada
* Author for correspondence (e-mail: Farrell{at}sfu.ca)
Accepted 18 June 2003
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Summary |
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Key words: salmon, Oncorhynchus nerka, Oncorhynchus kisutch, respirometry, energetics, temperature, oxygen consumption, critical swimming speed, fish stock, spawning run
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Introduction |
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Given the adult salmon's short migration window and its exposure to a wide
variation in temperature, it is possible that acclimation mechanisms that
would normally compensate for temperature change may be incomplete.
Conversely, Guderley and Blier
(1988) suggest that swimming
performance and most of its components demonstrate thermal compensation on an
evolutionary time scale (i.e. adaptation) such that optimal performance and
lowest thermal sensitivity are typically within the temperature range most
frequently encountered by the organism. In the case of adult salmon stock, the
prediction is that they would retain sufficient physiological flexibility to
accommodate the range of temperatures most frequently encountered during their
river migration; otherwise intolerance of non-optimal temperatures in reaching
spawning grounds (Macdonald et al.,
2000
) could hamper spawning success.
While considerable information on the temperature effects on swimming (e.g.
critical swimming speed, Ucrit) and oxygen consumption
(O2) exists for
juvenile Pacific salmon (Oncorhynchus spp.) (e.g.
Brett et al., 1958
;
Brett, 1971
;
Griffiths and Alderdice, 1972
;
Beamish, 1978
), only four
studies have measured
O2 in adult,
wild Pacific salmon (Brett and Glass,
1973
; Jain et al.,
1998
; Farrell et al.,
1998
,
2003
). One of these studies
(Brett and Glass, 1973
)
established a temperature optimum of 15°C for both
Ucrit and maximum
O2
(
O2max). All the
same, important intraspecific (between stocks) as well as interspecific
differences in swimming energetics with respect to temperature are
anticipated. Different salmon stocks migrate to different spawning streams in
the Fraser River watershed, resulting in dissimilar up-river migration costs
due to different water temperatures, coupled to variation in migration timing
as well as unequal migration distances in the presence of differing hydraulic
impediments. Indeed, juvenile salmonids reared or held under laboratory
conditions can show intraspecific differences among populations and strains
(Tsuyuki and Williscroft,
1977
; Thomas and Donahoo,
1977
; Taylor and McPhail,
1985
). Our focus was on whether performance differences exist
among adult, wild salmon stocks.
Berst and Simon (1981)
suggested that field-based rather than laboratory-based studies are more
likely to reveal any differences among species or stocks, because animal
transportation is minimized and natal river water can be used. While
Ucrit has been previously measured in adult salmonids
under field conditions (e.g. Jones et al.,
1974
; Brett, 1982
;
Williams et al., 1986
;
Farrell et al., 2003
), only
two field studies have previously reported active
O2 for adult
salmon (Farrell et al., 2003
;
C. G. Lee, A. P. Farrell and R. H. Devlin, manuscript submitted for
publication). Because no field study has comprehensively examined the effects
of temperature on swimming energetics in adult salmon, the present study
considered: (1) how the temperature affects swimming energetics of adult
salmon from the Fraser River watershed, and (2) whether intraspecific
differences in swimming energetics exist with respect to temperature. Assuming
that natural selection acts strongly on the physiology associated with
up-river migration, we predicted that swimming ability (as measured by
Ucrit and
O2max) should
increase with migration distance and difficulty among stocks of sockeye salmon
that were studied, one of which was a coastal (short-distance migrating) stock
while the other stocks (long-distance migrating) were from the interior of the
province of British Columbia (BC).
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Materials and methods |
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Field tests were always performed at ambient natal river water temperature and fish were transferred directly to the swim tunnel from the nearby stream or creek. Laboratory tests at both Simon Fraser University (with dechlorinated municipal water) and the Cultus Lake laboratory (with lake water) were performed either at the ambient temperature of the natal stream or at an adjusted temperature (Table 1). Laboratory-tested fish were transported in a 330 litre insulated tank containing oxygenated water, dilute Marinil anaesthetic (0.02 mg l1 metomidate hydrochloride, Syndel International Inc., Vancouver, BC, Canada) to calm the fish, and block ice to chill the water. Fish were held in 1000 litre aquaria, one of which was maintained at the ambient temperature of the fish's natal stream. The water temperature was adjusted (via mixing warm surface and cold deep Cultus Lake water) in the other aquaria at a rate of approximately 1°C per day over 5 days to extend the temperature range slightly beyond the ambient temperatures, after which two fish were tested daily in one of two swim tunnels receiving water at the fish's adjusted temperature. A longer temperature acclimation period was not used because some of these mature fish were within weeks of spawning. For all tests, fish were given a practice swim after 1 h and then allowed to recover in the swim tunnel overnight. Water delivery was at a rate of 30 l min1 via a submersible sump pump to ensure that dissolved oxygen was normally >90% of air saturation.
Gates Creek sockeye salmon: Seton Hydro dam and Cultus Lake
laboratory
Experiments were conducted on ten male and ten female adult GC sockeye
salmon at the BC Hydro Seton Dam near Lillooet, BC
(Fig. 1) in mid-August 2000.
Fish were dip-netted on-site at the top of a fish ladder and immediately
placed into a swim-tunnel. Fish, which were ripe and within 12 weeks of
spawning, were not killed after the experiments to comply with the sampling
permit and so gonad mass was not measured. In early August 2001, six male and
eleven female GC sockeye salmon were again collected at the Seton Dam site,
but were transported (1.5 h) to the Cultus Lake laboratory. Three fish were
tested at the ambient temperature of the Seton River at that time
(15.0±1.0°C), while six fish were tested at a colder and eight fish
at a warmer temperature.
Weaver Creek sockeye salmon: Chehalis River, and SFU and Cultus Lake
laboratories
Experiments were performed in October 2000 on six male and six female WVR
sockeye salmon at the Chehalis River Fish Hatchery, which is situated <5 km
from Weaver Creek, their natal stream. Fish were dip-netted at the spawning
creek, transported to the hatchery and immediately placed in the swim tunnel
for overnight recovery. Experiments were also conducted at Simon Fraser
University (SFU) on five male and seven female WVR sockeye salmon, captured by
beach seine from the Harrison River, BC, Canada
(Fig. 1) in September 2000.
Transportation to SFU took 1 h, where fish were held at 13.0±0.2°C
for a minimum of 3 days before testing commenced. An additional five male and
three female WVR sockeye salmon were collected from Weaver Creek via
dip-net and transported (0.5 h) to the Cultus Lake laboratory in October 2001.
Two fish were tested at the ambient water temperature at Weaver Creek
(12°C), while five fish were tested at a warmer temperature.
Early Stuart sockeye salmon: SFU laboratory
A small number of ES sockeye salmon were dip-netted from the Fraser River
near Yale, BC, Canada (Fig. 1)
in early July 2000, and transported (1.5 h) to SFU, where they were held for a
minimum of 3 days before testing commenced. These fish were 45 weeks
from spawning and were beginning to exhibit secondary sexual
characteristics.
Chehalis coho salmon: Chehalis River and Cultus Lake laboratory
Experiments were conducted in November 2000 on seven male and six female
CHE coho salmon that were captured with a knotless cotton dip-net from the
stream entering at the Chehalis River Fish Hatchery. Fish were immediately
placed into a swim tunnel for overnight recovery. Additional experiments were
conducted at the Chehalis River Fish Hatchery on six male and six female CHE
coho salmon in January 2001. Experiments were also conducted in November 2001
on four male and three female CHE coho salmon after transportation (0.5 h) to
Cultus Lake laboratory. Two fish were at the ambient temperature of the
Chehalis River (9°C), while five fish were tested at a warmer
temperature.
Swim tunnel
The 272 litre and 471 litre swim tunnels (after
Gehrke et al., 1990),
described in Farrell et al.
(2003
;
www.sfu.ca/biology/faculty/farrell/swimtunnel/swimtunnel.html)
were mounted on trailers to facilitate transportation to the field locations.
The 124.3 cm long transparent swim chamber had an internal diameter of 20.3 cm
for the small tunnel and 25.4 cm for the large swim tunnel. A `shocking' grid
(210 V; 0.42.0 W), made of graphite rods and mounted at the rear
of the swim chamber, was utilized briefly at higher water velocities to
promote swimming in some fish. Water flow in the swim tunnels was driven by a
29 cmdiameter fiberglass centrifugal impellor pump and a 7.5 hp three-phase
motor, controlled by a Siemens Midimaster Vector frequency drive (PLAD,
Coquitlam, BC, Canada). Water velocity was calibrated against the motor
frequency (Farrell et al.,
2003
). Throughout the course of an experiment, water temperature
in the swim tunnel did not fluctuate by more than 0.5°C.
Swim test protocol
The practice swim involved water velocity increments of 0.15 body lengths
(BL) s-1 every 2 min until failure and was used to
familiarize naïve fish to the swim tunnel and also provide an estimate of
the Ucrit (Jain et
al., 1997). The following day, each salmon was tested with a
ramp-Ucrit protocol
(Jain et al., 1997
), in which
the water velocity was ramped up in 5 min increments of 0.15 BL
s-1 up to approximately 50% of the fish's maximum speed attained in
the practice swim. Water velocity increments of 0.15 BL
s-1 then followed every 20 min until the fish ceased swimming.
Testing was terminated when the fish failed to move off the rear grid for 20
s. Water velocity was then reduced to 0.30-0.45 BL s-1 for
a 45 min recovery period, after which the a second
ramp-Ucrit protocol was performed. Approximately half the
fish swam intermittently as they recovered, while the remainder rested on the
bottom of the swim chamber for the entire recovery period.
Ucrit values were calculated as in Brett
(1965
):
Ucrit=Uf+(tf/tiUi),
where Uf is the water velocity of the last fully completed
increment; tf is the time spent on the last water velocity
increment; ti is the time period for each completed water
velocity increment (20 min); and Ui is the water velocity
increment (0.15 BL s-1). Ucrit was
corrected for the solid blocking effect as outlined by Bell and Terhune
(1970
). A streamline shape
factor was used in the correction equation
UF=UT(1+
s), where
UF is the corrected flow speed, UT is
the speed in the tunnel without a fish in the swim chamber and
s is the fractional error due to solid blocking.
s is defined for each fish by
s=
(Ao/AT)1.5,
where
is a dimensionless factor depending on swim chamber cross section
(equivalent to 0.8 in this study),
is the shape factor for the fish
(
=0.5 body length/body thickness), Ao is the cross
sectional area of the fish, and AT is the cross sectional
area for the swimming chamber. The Ucrit correction
averaged 16.2±0.1%. The second Ucrit test examined
the ability of fish to recover and re-perform. A recovery ratio (RR) expressed
the ratio of the two swimming performance tests:
RR=Ucrit2/Ucrit1. Thus, when RR=1, the
Ucrit performance was identical for both swim tests.
Oxygen consumption measurements
A Mark IV Oxyguard probe (Point Four Systems, Richmond, BC, Canada), housed
outside the swim tunnel in a flow-through, cylindrical housing (600 ml), was
used to measure oxygen concentration to 0.01 mg O2 l-1
in water delivered from the swim tunnel at a rate of 30 ml s-1
using a peristaltic pump (Masterflex, Cole Palmer, Vernon Hills, IL, USA). The
oxygen probe was air-calibrated daily and had automatic temperature
compensation. Early experiments used a stopwatch to time the decrease in
oxygen concentration, but subsequently signals were acquired by an in-house
computer program (Labview 6.0, National Instruments, Austin, Texas, USA) at a
sampling frequency of 0.2 Hz. Measurements of oxygen consumption lasted 5-20
min, depending on the fish's size and swimming speed, which was long enough to
record a change of 0.3-1.0 mg O2 l-1, but without
decreasing the dissolved oxygen concentration below 75% saturation during any
O2 measurement.
The swim tunnel was throughly flushed and bleached between experiments.
Biweekly assessments of background oxygen consumption without a fish in the
tunnel revealed no changes in the water oxygen concentration during a 20 min
recording period. The rate of oxygen consumption (mg O2
min-1 kg-1) was calculated as:
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Terminology and data analysis
The oxygen consumption measured immediately prior to the initial
Ucrit swim test was assigned as routine
O2
(
O2routine). We
did not attempt to estimate standard metabolic rate either by eliminating data
for fish that were active, as others have done (see
Brett and Groves, 1979
), or by
extrapolating to zero velocity, because of concerns regarding this method of
extrapolation (see Thorarensen et al.,
1993
; Farrell et al.,
2003
). Oxygen consumption rates during swimming were measured for
every other water velocity increment during both swim tests. The
O2 measured at
Ucrit was designated maximum
O2
(
O2max). We
distinguish
O2max from
active metabolic rate, which is defined as the
O2 during
maximum sustained activity (i.e. steady state swimming for >200 min;
Brett and Groves, 1979
). The
designation of
O2max during
swimming at Ucrit in salmonids was rationalized because
both cardiac output and venous oxygen partial pressure can plateau before
Ucrit is reached, and arterial oxygen partial pressure can
decrease (Thorarensen et al.,
1993
; Gallaugher et al.,
1995
; Farrell and Clutterham,
2003
). In addition, some fish can show a plateau in
O2 measurements
before Ucrit is reached (see data for GC sockeye). We did
not calculate metabolic scope (defined as active metabolic rate - standard
metabolic rate; Brett and Groves,
1979
). Instead, we calculated scope for activity (from
O2max-
O2routine).
Cost of transport, COT, was calculated from
O2/U
for each swimming speed, U, and net cost of transport,
COTnet, was calculated from
(
O2-
O2routine)/U.
The minimum costs of transport were interpolated from the curves fitted to
these data.
O2
measured immediately prior to the second Ucrit test was
termed
O2recovery, and
was compared with
O2routine to
determine the degree of recovery from the first swim test.
Statistical analysis
Values are means ± S.E.M. and P<0.05 was used
as the level of statistical significance. Intraspecific statistical
comparisons between the first and second swim trial and between the
laboratory-based and field-based measurements were performed with paired and
unpaired students t-tests, respectively. Statistical comparisons
among all fish stocks were accomplished using a parametric analysis of
variance (ANOVA). In cases where the ANOVA reported significant differences, a
pairwise post-hoc Tukey test was used to determine specifically which
groups were different. For the relationship between swimming speed U
and O2,
regression analysis used exponential equations, based on previous findings
(e.g. Webb, 1971
), although
preliminary analysis indicated that power functions (e.g. a 4-parameter
Lorentzian regression) also produced similar r2 values (to
within 10%). For the relationships with water temperature, exponential
regressions were used for
O2routine and
bell-shaped regression for
O2max and
Ucrit, based on previous findings
(Brett and Groves, 1979
).
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Results |
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ES sockeye salmon had a significantly higher Ucrit (P<0.05) than either GC or WVR sockeye salmon stocks but at a comparable ambient water temperature (Table 3). Conversely, CHE coho salmon swam as well as WVR sockeye (P>0.05), but at a lower ambient temperature (Table 3). Therefore, stock-specific differences existed independent of temperature differences.
Field versus laboratory testing
The swimming performance of some stocks did not vary between field and
laboratory tests (Tables 1,
2,
3). In addition, preliminary
laboratory experiments conducted with CHE coho salmon (N=4) showed
that routine O2,
Ucrit and
O2max
(2.59±0.14 mg O2 kg-1 min-1;
1.72±0.12 BL s-1; 9.19±0.61 mg O2
kg-1 min-1, respectively) were not statistically
different compared with field tests (Tables
1,
2,
3). Similarly, preliminary
laboratory experiments with GC sockeye salmon (N=4) showed that
Ucrit and
O2max
(2.15±0.11 BL s-1; 14.71±0.69 mg
O2 kg-1 min-1) were not statistically
different compared with field tests (Tables
2,
3), although
O2routine
(3.31±0.43 mg O2 kg-1 min-1) was
significantly (P<0.05) lower than field tests
(Table 2).
The two sets of field measurements for CHE coho salmon were pooled for
subsequent analyses because there were no significant differences (Tables
1,
2,
3). In contrast, WVR sockeye
salmon tested at the SFU laboratory had a significantly higher
Ucrit (23%),
O2max (19%) and
scope for activity (25%) compared with the same stock tested in the field when
the fish were in a slightly more mature state and also at a temperature
4°C colder (Tables 1,
2,
3). Consequently, the two data
sets for WVR sockeye salmon were treated separately for subsequent
analyses.
The effect of temperature on
O2routine
O2routine
measured at ambient temperature could vary significantly, but not always among
stocks, between years and between species
(Table 2). To investigate the
influence of ambient water temperature on
O2routine, all
stocks were pooled and a statistically significant (P<0.05)
exponential relationship existed between
O2routine and
ambient water temperature that accounted for 65% of the variation in the
individual data (Fig. 2).
Addition of temperature-adjusted fish to this pooled data set slightly
weakened the relationship (r2=0.52; P<0.05)
(Fig. 2).
|
The effect of temperature on
O2max, scope
for activity and Ucrit
Regression analysis was performed for three salmon stocks (GC, WVR and
CHE), revealing significant (P<0.05) bell-shaped relationships
between O2max
and temperature (Fig. 3A) when
data from temperature-adjusted fish were included. Temperature optima for
O2max were
interpolated from the regression equations (GC=17.5°C; WVR=15.0°C;
CHE=8.5°C) and were found to correspond closely to the ambient water
temperature for each stock (Table
1; Fig. 3A).
Furthermore, when individual
O2max values
were compared among sockeye stocks and at common ambient temperatures, there
were clear differences between stocks (Fig.
3A). These results suggest that important stock-specific
differences existed for
O2max and its
thermal sensitivity. Similarly, significant (P<0.05) bell-shaped
regressions were found between scope for activity and temperature for each
salmon stock (Fig. 3B). The
temperature optimum for scope for activity was either similar to that for
O2max (CHE
stock), or 1°C lower (WVR and GC stocks)
(Fig. 3B), reflecting the
important contribution of temperature on
O2routine.
|
For GC and WVR sockeye salmon stocks, there were significant (P<0.05) bell-shaped regressions between Ucrit and temperature, with Ucrit falling off at temperatures >19°C and >16°C, respectively (Fig. 4). For CHE coho salmon, the regression between Ucrit and temperature was not significant (P=0.71) (Fig. 4).
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Oxygen cost of transport
The increase in
O2 with swimming
speed is illustrated for three salmon stocks from the various test locations
(Fig. 5A). As expected,
O2 varied
exponentially (r2=0.99) with swimming speed for WVR
sockeye salmon and CHE coho salmon. However, for GC sockeye, the data were not
satisfactorily fitted by an exponential relationship and a sigmoidal
regression (r2=0.99) was required to account for the
plateau in
O2
prior to Ucrit. Only
O2routine and
O2max were
measured for ES sockeye salmon and these values are included in
Fig. 5A-C.
|
O2 differed
significantly (P<0.05) among the salmon stocks at intermediate
swimming velocities, with GC sockeye salmon having the highest
O2 values and
CHE coho salmon the lowest values for a given swimming velocity. The cost of
transport showed typical U-shaped curves with the exception of GC sockeye
salmon (Fig. 5B), because GC
sockeye salmon were tested at the highest temperature and
O2routine
increased exponentially with temperature. GC sockeye salmon were the least
economical swimmers. The difference among stocks could simply reflect a higher
O2routine.
However, this was found not to be the case because the net cost of transport
was also elevated for GC sockeye salmon
(Fig. 5C). In contrast, because
WVR sockeye salmon and CHE coho salmon had a similar net cost of transport,
the small differences in the cost of transport between these two stocks were
likely a result of temperature effects on
O2routine. The
minimum cost of transport occurred at around 1 BL s-1 for
all three salmon stocks (Fig.
5B).
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Discussion |
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Although the blocking effect for a few of the fish was high, the
Ucrit and
O2max data
obtained here for sockeye salmon are entirely consistent with earlier
laboratory and field studies involving adult Pacific salmon (e.g.
Brett and Glass, 1973
;
Jones et al., 1974
;
Williams et al., 1986
). For
example, Ucrit (2.41 BL s-1,
N=8) reported for smaller (1.65±0.07 kg) adult sockeye salmon
(Brett and Glass, 1973
) lies
in the upper end of our Ucrit range, while our
O2max data tend
to be higher than theirs at corresponding temperatures
(Fig. 3C).
O2max (13.83 mg
O2 kg-1 min-1) and Ucrit
(2.33 BL s-1) for pink salmon
(Williams et al., 1986
) are
comparable to the present study. The exponential relationships between
O2max and
temperature reported earlier for adult sockeye salmon either lie below
(Davis, 1966
) or above
(Brett and Glass, 1973
) a
significant exponential relationship (r2=0.63;
Fig. 3C) that could be fitted
to our
O2max
data. (Note: this exponential regression tended to over-represent WVR sockeye
salmon and under-represent both ES and GC sockeye salmon, i.e. there was a
poor fit for any of the individual salmon stocks.) The high quality of the
present data was also illustrated by the repeatability of the swim tests,
because RR decreases significantly (Jain
et al., 1998
; Tierney,
2000
) when rainbow trout Oncorhynchus mykiss and sockeye
salmon are either sick or have been challenged by toxicants.
Temperature effects
The final temperature preferendum paradigm, proposed by Fry
(1947), embodied three
principal inferences: a species-specificity to the final temperature
preferendum; a relationship between the final temperature preferendum and
field distribution; and a relationship between final temperature preferendum
and the temperature at which centrally important processes take place at
maximum efficiency. Indeed, the concept of temperature optima for
physiological processes related to swimming is well documented (see reviews by
Beamish, 1978
;
Houston, 1982
;
Guderley and Blier, 1988
;
Hammer, 1995
;
Kelsch, 1996
;
Johnston and Ball, 1997
;
Kieffer, 2000
). Furthermore,
there is emerging evidence that maximum cardiac performance and the oxygen
supplying the cardiac tissue may be `centrally important processes' (Farrell,
1997
,
2002
), though other processes
are likely to be important (Pörtner,
2002
). The present results therefore extend the idea of
temperature optima to include the possibility of stock-specific temperature
optima, in addition to confirming an important temperature effect on the
physiological processes that determine
O2max, scope for
activity and Ucrit. Three stocks of adult salmon
demonstrated distinct temperature optima for
O2max and scope
for activity, while GC and WVR sockeye salmon also exhibited temperature
optima for Ucrit. In contrast, Ucrit
for CHE coho salmon displayed low temperature sensitivity. Temperature optima
around 15°C have been reported previously for
O2, metabolic
scope and sustained cruising speed with juvenile and adult sockeye salmon
(Brett and Glass, 1973
). While
this temperature is very close to the temperature optima reported here for GC
sockeye salmon, there were clear differences in the temperature optima for WVR
sockeye salmon (Fig. 3).
Furthermore, the temperature optima adult CHE coho salmon are considerably
lower than that reported earlier for juvenile coho salmon (approx. 20°C;
Brett et al., 1958
), a
difference that could reflect either a stock-specific effect or developmental
effect.
Although temperature optima were clearly established for the salmon stocks,
a measure of temperature insensitivity for peak swimming capability is likely
to be critical for these salmon stocks because they routinely face varying
water temperatures. To gauge temperature insensitivity we used the regression
equations to arbitrarily estimate the temperature range over which a salmon
stock could reach at least 90% of its peak
O2max. These
temperature ranges were: 14.7-20.3°C for GC sockeye salmon,
12.7-17.3°C for WVR sockeye salmon and 5.0-11.4°C for CHE coho salmon.
Using a similar analysis for scope for activity, the temperature ranges for
the three stocks were similar to those for
O2max, but
marginally cooler and/or narrower (13.9-19.3°C for GC sockeye salmon,
12.8-16.2°C for WVR sockeye salmon and 6.6-8.9°C for CHE coho salmon).
This analysis clearly shows that these three salmon stocks can approach their
respective peak aerobic activity over a temperature range spanning as much as
5°C. Such physiological flexibility may be adaptive (see Guderley and
Blier, 1998) because the water temperature in the Fraser River may vary
annually on a given date by as much as 6°C, perhaps even providing
sufficient flexibility to handle all but the most extreme temperature
conditions encountered in the Fraser River during a particular migration
window. This does not mean that extreme temperature and/or hydrological
conditions (known to occur in certain years) would not impose difficulties for
migration (e.g. ES sockeye have faced water temperatures reaching 22°C and
flows of 9000 m3 s1;
Macdonald et al., 2000
). But
it does mean that physiological information provided here could be useful in
predicting which river conditions are more likely to impair passage and reduce
spawning success.
An equally important discovery was that these temperature optima correlated
very closely with the ambient water temperature of the natal river for
individual salmon stocks. This meant that the lowest thermal sensitivity of
peak aerobic performance occurred around the ambient temperature of the natal
stream. While environmental variability can differentially influence the
ability of organisms to survive and reproduce, tailoring populations to their
respective environmental niches (Cooke et
al., 2001), and the `stock concept' suggests adaptation to local
conditions (Berst and Simon,
1981
), migratory salmon spend most of their life away from the
natal streams. Whether the present correlation between temperature optima and
natal stream temperature is a reflection of adult salmon being pre-adapted to
water temperatures likely to be encountered during river migrations, or is
coincidental with the temperature preferendum of the species (e.g. for sockeye
salmon 14.5°C, Brett, 1952
;
10.6-12.8°C, Horak and Tanner,
1964
), will require further study. Further work will also need to
tackle the possibility of rather rapid thermal compensation during the actual
in-river migration. For some sockeye salmon stocks, the timing of migration
seems to have been far too restrictive for thermal compensatory processes to
take full effect. For example, ES sockeye move from seawater in the Georgia
Strait, where they encounter temperatures likely to be no warmer than
13°C, into river water as high as 18°C, and then within 4 days face
one of their most difficult in-river swimming challenges, Hell's Gate.
Although the majority of tests were performed at ambient water temperature,
small temperature adjustments were used to extend the ambient temperature
range. Acclimations to these temperatures were necessarily short (5 days)
because fully ripe salmon have compromised swimming ability
(Williams et al., 1986). While
the short acclimation period is a concern, the extent of the temperature
change (<6°C) was not unusual compared with changes naturally
encountered, because ES and Chilko stocks of adult sockeye salmon routinely
face temperature changes of 1°C daily and as much as 7°C over 1 day
during their migrations (Idler and
Clemens, 1959
). In addition, individual fish tested at either
their ambient temperature or an adjusted temperature showed a reasonable
overlap of
O2max
values (Fig. 3A). A second
concern is that we did not consider sex differences in swimming energetics.
This concern is offset by the fact that we used equal numbers of male and
female fish in many test groups. Furthermore, physiological telemetry studies
of migrating ES sockeye salmon and Seton River pink salmon have revealed
little difference between sexes in terms of the overall cost of transport to
the spawning site, although males were less efficient at migrating through
hydraulic obstacles (Hinch and Rand,
1998
; Standen et al., 2002). The present study could be used as a
framework for future studies of sexual dichotomy in swimming capabilities.
The finding that
O2routine
increased exponentially with temperature is consistent with previous studies
showing exponential relationships for both
O2routine and
standard metabolic rate (rainbow trout;
Dickson and Kramer, 1971
),
brown trout Salmo trutta; Butler
et al., 1992
), sockeye salmon
(Brett and Glass, 1973
),
tilapia Sarotherodon mossambicus;
Caulton, 1978
) and largemouth
bass Micropterus salmoides; Cooke
et al., 2001
). As expected, our
O2routine values
for adult sockeye salmon were higher than the standard metabolic rate
previously reported (Brett and Glass,
1973
). Some of this difference could be attributed to the on-going
gonadal development in the mature fish used in the present study. It is also
possible that the overnight recovery is insufficient (see
Farrell et al., 2003
) and
adult salmon are more restless than less mature fish. Williams et al.
(1986
) noted that adult pink
salmon were more restless than sockeye salmon in swim tunnels.
Intraspecific differences in relation to migration distance and
difficulty
The intraspecific differences in migration capacity were sometimes
correlated with in-river migration distance and difficulty. For example, ES
sockeye salmon, the furthest migrating stock of any of the Fraser River
salmon, attained a significantly higher Ucrit at a 5°C
cooler temperature and were more efficient swimmers at
Ucrit because of a lower
O2max compared
with GC sockeye salmon. These attributes of ES sockeye salmon may be
advantageous because they migrate almost three times the distance up the
Fraser River compared with GC sockeye salmon
(Table 1). Similarly, both ES
and GC sockeye salmon migrate much longer distances and negotiate more severe
hydraulic challenges compared with the coastal WVR sockeye salmon and
correspondingly had a larger scope for activity at comparable water
temperatures. Moreover, almost all of the GC and ES fish repeated their
swimming performance without recovering
O2 to within 5%
of
O2routine.
The differences in swimming energetics found between CHE coho salmon and WVR
sockeye also probably reflect species-specific adaptations. Yet, because these
two salmon stocks face almost identical in-river migration distances and
conditions, other factors must be involved in these adaptations. Thus, the
suggestion that distance and/or difficulty of migration are powerful selective
factors acting on salmonids (Bernatchez and
Dodson, 1985
; G. T. Crossin, S. G. Hinch, A. P. Farrell, D. A.
Higgs, A. G. Lotto, J. D. Oakes and M. C. Healey, unpublished observations) is
supported by the present study.
Intraspecific adaptation of maximum swimming ability has been previously
established for juvenile salmonids either held or reared in a laboratory, but
to our knowledge not for adult, wild salmon. For example, juvenile Pacific
coho salmon from an interior river had an inheritable trait that resulted in a
lower initial acceleration for a fast start, but a longer time-to-fatigue at a
constant swimming speed compared with coho salmon from a coastal river
(Taylor and McPhail, 1985).
Similarly, Pacific steelhead trout O. mykiss from an interior river
also had a greater time-to-fatigue for an incremental swimming speed test and
allelic differences in the lactate dehydrogenases compared with a coastal
stock (Tsuyuki and Williscroft,
1977
). Nevertheless, because Bams
(1967
) found that rearing
conditions could alter swimming performance of sockeye salmon fry, phenotypic
rather than genotypic expression could have contributed to the differences we
observed.
Paradoxically, GC sockeye salmon were less efficient swimmers than either
WVR sockeye salmon or CHE coho salmon, and why this is so is unclear. GC
sockeye salmon were unusual in another regard, the plateau in
O2 as the fish
neared Ucrit. In fish,
O2 typically
increases exponentially with swimming speed (see
Beamish, 1978
) to overcome
drag, which is exponentially related to water velocity
(Webb, 1975
). Rarely is a
plateau observed in
O2 even though
fish progressively increase the anaerobic contribution to swimming at 75%
Ucrit (Brett and
Groves, 1979
; Burgetz et al.,
1998
). Consequently, the plateaus for both
O2 and the cost
of transport curve near Ucrit for GC sockeye salmon point
to an unusually high contribution of anaerobically fueled locomotion. This
possibility is further explored in the accompanying paper
(Lee et al., 2003b
), in which
excess post-exercise oxygen consumption is examined as a measure of the
anaerobic swimming activity.
In summary, we conclude that variation in
O2routine among
adult salmon stocks was primarily due to differences in water temperature. In
contrast, distinct temperature optima for
O2max were
evident among salmon stocks, which when combined with differences in scope for
activity and Ucrit, suggest stock-specific as well as
species-specific differences in the temperature sensitivity of the
physiological mechanisms that underpin oxygen delivery during swimming in
adult Pacific salmon.
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