Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus
Department of Biological Science, California State University
Fullerton, Fullerton, CA 92834, USA
Present address: Marine Biology Research Division, Scripps Institution of
Oceanography, University of California San Diego, La Jolla, CA 92093,
USA
Present address: Anaheim High School, 811 W. Lincoln Avenue, Anaheim, CA
92805, USA
* Author for correspondence (e-mail: kdickson{at}fullerton.edu )
Accepted 24 January 2002
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Summary |
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Key words: Scombridae, chub mackerel, Scomber japonicus, locomotion, kinematics, cost of transport, metabolism, sustained swimming, energetics, respirometer, temperature
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Introduction |
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Quantifying the effects of temperature on swimming performance is important
for active ectothermic species such as S. japonicus that experience
wide ambient temperature ranges as well as for the few endothermic fish
species that maintain the temperature (Tm) of their
slow-twitch, oxidative locomotor muscle significantly above water temperature.
Among teleost fishes, only the tunas have been documented to maintain an
elevated Tm using vascular counter-current heat exchangers
(Carey et al., 1971) (for a
review, see Block, 1991
).
Steady-state Tm values measured by acoustic telemetry in
tunas are elevated above water temperature by as much as 6-13°C
(Carey and Lawson, 1973
;
Holland et al., 1992
;
Stevens et al., 2000
;
Marcinek et al., 2001
).
Although it has been hypothesized that elevating Tm
enhances swimming performance in tunas, no study has yet been able to test
this hypothesis directly by comparing the swimming performance of tunas
possessing significantly elevated muscle temperatures with that of closely
related ectothermic fishes of similar size (see
Sepulveda and Dickson, 2000
).
Because the ectothermic chub mackerel and the tunas are members of the family
Scombridae, the effects of temperature on swimming in the chub mackerel may be
used to model the potential enhancing effects of maintaining an elevated
Tm on sustainable swimming performance in tunas. The
present study examined continuous swimming, which is assumed to be powered by
the slow-twitch, oxidative myotomal muscle (for reviews, see
Rome, 1995
;
Jayne and Lauder, 1996
;
Webb, 1998
) because that
muscle is perfused via vascular counter-current heat exchangers and
maintained at significantly elevated temperatures in the tunas
(Carey et al., 1971
).
Several previous studies that have quantified the effects of temperature on
continuous swimming in teleost fishes have shown that metabolic rate and
maximum sustainable swimming speed generally increase with temperature [e.g.
in sockeye salmon Oncorhynchus nerka
(Brett and Glass, 1973); carp
Cyprinus carpio (Rome et al.,
1984
); scup Stenotomus chrysops
(Rome et al., 1992
); striped
bass Morone saxatilis (Sisson and
Sidell, 1987
); rainbow trout Oncorhynchus mykiss
(Kieffer et al., 1998
);
Atlantic menhaden Brevoortia tyrannus
(Macy et al., 1999
)]. In some
cases, there is a decrease in these variables at high temperatures that
approach the maximum environmental temperature experienced by the species
[sockeye salmon (Brett and Glass,
1973
); juvenile walleye Stizostedion vitreum vitreum
(Beamish, 1990
); rainbow trout
(Taylor et al., 1996
)].
Surprisingly, some studies have failed to show a significant effect of
temperature on sustainable swimming performance [e.g. for the delta smelt
Hypomesus transpacificus (Swanson
et al., 1998
)].
Fewer studies of the effects of temperature on the kinematics of sustained
swimming in teleosts exist, but most show small or insignificant effects. At a
given sustainable speed, neither tail-beat frequency nor tail-beat amplitude
varied with temperature in carp (Rome and
Sosnicki, 1990). Similarly, no temperature effect on tail-beat
frequency was found in scup (Rome et al.,
1992
) or in goldfish Carassius auratus
(Smit et al., 1974
). However,
the tail-beat frequency versus swimming speed relationships varied
with temperature in rainbow trout
(Stevens, 1979
;
Taylor et al., 1996
),
largemouth bass Micropterus salmoides
(Stevens, 1979
) and striped
bass (Sisson and Sidell,
1987
), and Swank and Rome
(2000
) found a small but
significant increase at 20°C compared with 10°C in tail-beat frequency
measured at a swimming speed of 50 cm s-1 but not at 40 cm
s-1 for scup. The latter findings suggest that swimming efficiency
may change with temperature.
We know of no published study that has simultaneously examined the effects
of temperature on sustainable swimming, swimming energetics and swimming
kinematics for a species as well adapted for rapid and continuous swimming as
the chub mackerel. Thus, the objective of the present study was to compare the
previously reported data for chub mackerel at 24°C
(Donley and Dickson, 2000;
Sepulveda and Dickson, 2000
)
with data for the same species at 18°C to determine the effect of a
temperature change of that magnitude on sustainable swimming performance and
swimming kinematics of scombrid fishes.
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Materials and methods |
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Respirometry
All experiments were conducted in a Brett-type, temperature-controlled,
variable-speed respirometer containing a total volume of 35 litre (13.5
cmx27.0 cmx101.6 cm), as described previously
(Donley and Dickson, 2000;
Sepulveda and Dickson, 2000
).
Individual fish swam against water currents of known velocities, determined by
calibration with a General Oceanics mechanical flow meter (model 2030 R).
Corrections for solid blocking effects were not necessary because all fish had
maximal cross-sectional areas that were less than 10% of the cross-sectional
area of the 13.5 cmx13.5 cmx50.8 cm fish test chamber
(Brett, 1964
;
Webb, 1971
). Each fish was
removed from the holding tank by capture with a baited, barbless hook and
placed, with minimal handling, into the respirometer. Before starting an
experiment, each fish was allowed to adjust to the respirometer chamber for 4h
in the case of the 24°C mackerels or for 12-19h (overnight) for the
18°C mackerels. Water temperature within the respirometer system was
maintained at 18.4±0.2°C or 24.0±0.2°C, respectively,
with an in-line heater and chiller system.
Maximum sustainable swimming speed
In total, 12 chub mackerel at each temperature [15.6-26.3 cm fork length
(FL) (20.9±4.0 cm, mean ± S.D.) and 34-179 g at
18°C; 14.0-24.7 cm FL (20.3±3.4 cm) and 26-156 g at
24°C] were used in swimming performance experiments. A modification of the
Brett (1964) procedure for
measuring critical swimming speed (Ucrit) was used to
determine the maximum sustainable speed. Each fish was forced to swim for
sequential 30-min periods at specific speeds, starting at 15-40 cm
s-1. Speed was increased in increments of 7.5 or 10 cm
s-1. We attempted to use a speed increment of approximately 10% of
the expected maximum sustainable speed; the increments were actually
10.7±1.7% and 10.8±1.9% (mean ± S.D.) of that value for
fish at 18°C and 24°C, respectively. The maximum speed that each fish
was able to maintain for an entire 30-min period while swimming using a gait
characterized by steady, continuous tail beats (Umax,c),
assumed to be powered by the slow-twitch, oxidative myotomal muscle, was
determined.
Several investigators have shown that the aerobic myotomal muscle powers
sustainable swimming in fish and that recruitment of the fast-twitch,
glycolytic muscle fibers at higher speeds is evident in a change in gait from
a continuous tail beat to intermittent bursts of high-frequency tail beats
followed by gliding (for reviews, see
Videler, 1993;
Rome, 1995
;
Webb, 1998
). Thus, when the
fish shifted from a steady tail beat to a `burst-and-glide' gait three times
within 30s, we assumed that it could not maintain speed using the aerobic
muscle alone and had to recruit the fast-twitch muscle fibers. The preceding
speed that the fish had maintained for 30 min was designated as
Umax,c (maximum continuous or cruising speed) for that
fish. Thus, Umax,c values in the present study are lower
than Ucrit values determined using the Brett
(1964
) formula, which takes
into account the period the fish swam at the speed at which it switched to
burst-and-glide swimming.
Swimming energetics
Fish oxygen consumption rate
(O2) was
measured at each speed during the Umax,c trials using a
Yellow Springs Instruments polarographic oxygen electrode and meter connected
to a chart recorder, as described by Sepulveda and Dickson
(2000
).
O2 was measured
during the middle 10-27 min of each 30-min period at each speed; the time
required depended upon the fish's
O2 and thus
varied with fish size, speed and temperature. The minimum level of oxygen
saturation in the respirometer for all trials for each fish was 79-95% at
18°C and 88-98% at 24°C, and all tracings of water oxygen
concentration versus time were linear. During the remainder of the
30-min period at each speed, the respirometer water oxygen content was brought
back to the original 100% saturation level by allowing water to flow to and
from a reservoir of oxygenated or aerated sea water connected to the
respirometer by a valve system. The valves to the reservoir were closed
whenever
O2 was
measured. After each experiment, the fish was removed and the respirometer was
re-sealed for the determination of the background respiration rate, which was
subtracted from all
O2 measurement
to determine fish
O2 at each
speed.
The net cost of transport (COTnet, in J km-1
kg-1), or incremental cost of swimming, was calculated by plotting
O2
versus swimming speed for each fish. The slope of the best-fitting
linear regression of the resulting graph is proportional to the average net
cost of transport for the fish (see
Sepulveda and Dickson, 2000
).
The slope units (mg O2 min-1 cm-1 s) were
multiplied by (1 minx60 s-1) to remove time and then
converted to J km-1 kg-1 by multiplying by 13.54 J
mg-1 O2 and dividing by fish mass.
Each fish's standard metabolic rate (SMR) was estimated by extrapolating
the logO2
versus swimming speed relationship to zero speed. Although these
estimates are associated with considerable error, it has been shown for tunas
that SMRs calculated in this way are similar to oxygen consumption rates of
paralyzed, restrained individuals (Brill,
1987
; Dewar and Graham,
1994
).
Swimming kinematics
Individual chub mackerel were videotaped at 120 Hz using a Peak Performance
Technologies high-speed video camera (model TM640) positioned in front of a
mirror mounted at 45° above the respirometer to obtain a dorsal view of
the fish. The swimming kinematics of 13 chub mackerel (15.6-26.3 cm
FL) at 18°C and eight chub mackerel (14.0-23.4 cm FL) at
24°C were analyzed. Video recordings were made onto Maxell Professional
SVHS tapes over a 2- to 10-min period at each speed at which the fish swam
during its O2
measurements. Videotapes were analyzed using a Peak Performance Technologies
two-dimensional motion-analysis system, as described by Donley and Dickson
(2000
).
Video segments in which the fish was swimming steadily for 8-10 tail beats
and was positioned in the center of the chamber, away from the walls and
bottom of the chamber, were selected for analysis. Six points along the dorsal
midline of each fish that could be identified consistently were digitized in
sequential video fields for 8-10 tail beats at each speed: the tip of the
snout, the points along the dorsal midline between both the anterior and the
posterior insertion points of the eyes, the midpoint between the anterior
insertions of the pectoral fins, the caudal peduncle and the tip of the upper
lobe of the caudal fin. The kinematic variables tail-beat frequency, tail-beat
amplitude, stride length (the distance traveled per tail beat) and propulsive
wavelength were calculated for each individual at each speed by analyzing the
progression of these digitized points over time, as described by Donley and
Dickson (2000). Propulsive
wave velocity (C), the speed of the wave of undulation that travels
down the body during swimming, was calculated from the time (s) between the
peaks in lateral displacement at two points, the tip of the snout and the tip
of the tail. For each individual at each speed, 7-10 measurements were
averaged to calculate progression time. The distance between the two points
(which is equal to fish total length) was divided by the average progression
time to obtain the propulsive wave velocity (C) in cm s-1
at each speed for each individual. Propulsive wavelength (
) was
calculated by dividing C by the fish's tail-beat frequency at that
speed.
Statistical analyses
Differences between the two mackerel groups in the relationships between
Umax,c, COTnet or SMR and fish size (both fork
length and mass) were assessed using a general linear model (GLM) analysis of
covariance (ANCOVA) in Minitab (version 10.5). Because speed and size covary
and both may affect
O2 and each of
the kinematic variables, it was necessary to use a multivariate analysis to
determine whether temperature had a significant effect on these variables (see
Donley and Dickson, 2000
). We
determined whether there was a significant difference between the two mackerel
groups, indicating a significant effect of temperature, in the relationship
between each variable and swimming speed and fish size. After determining that
the data were normally distributed and thus did not need to be transformed, a
repeated-measures multiple regression analysis (ANCOVA) was performed with SAS
(version 6.12) using the regression equation for chub mackerel at 24 °C as
a baseline with which the corresponding regression for the 18 °C mackerel
was compared. Each variable was tested for the effects of temperature, speed
and fish size, in terms of both mass and fork length, all possible two-way and
three-way interactions and a four-way interaction term.
Unless indicated, values are presented as means ± S.D.
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Results |
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Swimming energetics
In the chub mackerel at both temperatures, the rate of oxygen consumption
(O2 in mg
O2 min-1) increased significantly with both fish mass
and swimming speed. At a given speed and fish size,
O2 was
significantly higher at 24 than at 18 °C
(Fig. 2). These findings are
best represented by three-dimensional, multivariate plots of
O2 as a function
of both fish mass and speed at the two temperatures
(Fig. 3;
Table 2). The multivariate
ANCOVA indicated significant effects of temperature, speed and fish mass on
O2, as well as a
significant interaction between speed and temperature (for all,
P<0.0001). There was a greater rate of increase in
O2 with speed at
24 than at 18 °C (Fig. 3;
Table 2). When the effects of
speed and mass are taken into account, there was no significant effect of
FL on
O2
(P=0.18).
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At a given fish size, the incremental cost of swimming or net cost of
transport (COTnet), which is proportional to the slope of the
O2
versus swimming speed regression for each individual
(Fig. 2), was significantly
greater at 24 than at 18 °C (P=0.02, ANCOVA)
(Fig. 4). This is reflected in
the significant speed x temperature interaction term in the multivariate
analysis for
O2.
At both temperatures, mass-specific COTnet decreased with fish
FL (Fig. 4) and with
fish mass (Table 1) but, when
the effect of FL was accounted for, there was no significant effect
of fish mass on COTnet (ANCOVA).
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The mass-specific SMRs, estimated from the coefficient a in the
exponential O2
versus swimming speed curves (the y-intercept of the
log
O2
versus swimming speed regression) for each individual
(Fig. 2), ranged from 38.6 to
290.2 mg O2 h-1 kg-1 (mean 126.4±67.2
mg O2 h-1 kg-1, N=12) at 18 °C
and from 53.2 to 280.0 mg O2 h-1 kg-1 (mean
143.2±80.3 mg O2 h-1 kg-1,
N=12) at 24 °C. There was a significant effect of mass on SMR
when expressed as mg O2 min-1 (P<0.001), but
not when expressed as mg O2 h-1 kg-1. There
was no significant effect of temperature on the relationship between SMR (mg
O2 h-1 kg-1) and fish mass (ANCOVA) or on the
mean mass-specific SMR (t-test).
Swimming kinematics
When the effects of fish size were accounted for, tail-beat frequency
increased significantly with speed at both temperatures (P<0.0001)
at the same rate (Table 2;
Fig. 5). When the effects of
speed were taken into account, there was a significant effect of FL
on tail-beat frequency (P<0.0001)
(Table 2;
Fig. 5). The rate of decrease
in tail-beat frequency with FL did not vary with temperature
(Fig. 5). When the effects of
speed and fork length were accounted for, neither mass nor temperature had a
significant effect on tail-beat frequency. Thus, at both temperatures, chub
mackerel of a given size use the same tail-beat frequency to swim at a given
speed.
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The effects of fish size, swimming speed and temperature on tail-beat amplitude, expressed both in absolute units (cm) and relative to fish size (as a percentage of FL, % FL), were examined. In both mackerel groups, tail-beat amplitude (in both cm and % FL) increased significantly with speed (P<0.0001) and tail-beat amplitude (in cm) increased with FL (P<0.0001) (Table 2; Fig. 6). The rates of increase in tail-beat amplitude with speed and with FL were not affected by temperature (Fig. 6). When speed and fork length were accounted for, there was no significant effect of mass on tail-beat amplitude (in cm or % FL). When expressed as a percentage of FL, there was no significant effect of fish size on tail-beat amplitude (Table 2), indicating that dividing tail-beat amplitude by fish length was an appropriate adjustment for size differences in both groups of chub mackerel. When the effects of speed and fork length were accounted for, there was no significant effect of temperature on tail-beat amplitude (in cm or % FL) (Table 2; Fig. 6).
|
Stride length (l) increased significantly with speed (P<0.0001) and with FL (P<0.0001) at both temperatures (Table 2; Fig. 7). When the effects of speed and FL were accounted for, there was no significant effect of fish mass on l. The slopes of the regressions of l versus speed and of l versus FL did not differ with temperature. When the effects of speed and fork length were accounted for, there was no significant effect of temperature on l (Fig. 7).
|
There were significant effects of temperature (P=0.0024) and
FL (P<0.0001), but not of speed or mass, on the
propulsive wavelength () (Table
2). Thus, the relationship between the mean
for each
individual and fish FL was compared at the two temperatures. At a
given fish size, mean
was significantly greater at 24 than at 18
°C (Fig. 8). The rate of
increase in
with FL was the same at both temperatures
(Fig. 8).
|
When the data for the 24 °C chub mackerel were analyzed previously
(Donley and Dickson, 2000),
there were significant effects of fish FL on both relative stride
length and relative propulsive wavelength expressed as a percentage of
FL. This indicates that attempting to normalize stride lengths and
propulsive wavelengths for fish size by dividing by FL introduces a
different size effect to the data and, thus, may result in misleading
conclusions (see Packard and Boardman,
1999
). Therefore, we have not included analyses of the relative
(size-specific) values of these two kinematic variables.
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Discussion |
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Sepulveda and Dickson
(2000) showed that, at 24
°C, the SMR for S. japonicus was lower than that for
similar-sized kawakawa tuna, but the SMR values measured in the present study
are similar to or somewhat higher than those reported for other active
teleosts of similar size at similar temperatures. For example, SMRs of 73 mg
O2 h-1 kg-1 were measured in menhaden
(303±38 g) acclimated to and measured at 15 °C, and those
(283±40 g) acclimated to and measured at 20 °C had SMRs of 87 mg
O2 h-1 kg-1
(Macy et al., 1999
). Freadman
(1979
) measured an SMR of 156
mg O2 h-1 kg-1 at 15 °C in 217 g
bluefish, Pomatomus saltatrix, and the values estimated from
Fig. 3 of Brett and Glass
(1973
) for sockeye salmon of
the same mass as the mackerel in the present study are 90-110 mg O2
h-1 kg-1 at 18 °C and 140-190 mg O2
h-1 kg-1 at 24 °C.
Maximal sustainable speeds have been measured previously in mackerel.
Atlantic mackerel S. scombrus (29-33 cm FL), swimming in a
circular gantry tank and stimulated to swim at different speeds by the
optomotor response, could maintain a speed of 4.1 FL s-1
(120-137 cm s-1) for 30 min at 11.7 °C
(He and Wardle, 1988). If the
Umax,c versus FL regressions in
Fig. 1 are extrapolated to that
size range, these values fall between the lines for 18 and 24 °C and,
thus, are higher than the present study would predict. Roberts and Graham
(1979
) swam S.
japonicus (34.3-39.2 cm FL) at maximum speeds of 3.2-4.5
FL s-1 (125-171 cm s-1) in a swimming tunnel 12
cm in diameter at 16.1-21.8 °C. The time for which each fish swam at those
speeds was not explicitly stated, but was apparently 3 min. These values fall
close to the Umax,c versus FL regression for chub
mackerel at 24 °C, when extrapolated to the higher FL values. The
maximum sustainable swimming speeds ranged from 2.75 to 3.25 FL
s-1 (70-86 cm s-1) for 24-28 cm FL S. japonicus
at 14-15 °C (Shadwick and Steffensen,
2000
) (R. E. Shadwick, personal communication), comparable with
the values of 67.5-97.5 cm s-1 (2.6-3.9 FL s-1)
for 24.8-26.3 cm FL S. japonicus at 18 °C in the present study.
Thus, the Umax,c values for a given temperature and fish
size in the present study appear to be somewhat lower than the only other
values for Scomber spp. that we could find, but methodological
differences could at least partially account for this.
The Umax,c values measured in S. japonicus are
similar to those reported for other active teleost fishes of similar size at
similar temperatures. Sepulveda and Dickson
(2000) showed that, at 24
°C, the Umax,c for S. japonicus did not
differ significantly from that measured in similar-sized kawakawa tuna. We
have measured Umax,c values of 74-118 cm s-1 at
27 °C for 19.1-26.0 cm green jack Caranx caballus in the same
respirometer system (K. A. Dickson, M. W. Hansen, J. M. Donley and J. A.
Hoskinson, unpublished results). At 13.5 °C, 25.3 cm herring, Clupea
harengus, could maintain a speed of 121 cm s-1 for 30 min and,
at 14.4 °C, 25.5 cm saithe, Pollachius virens, could maintain a
speed of 98 cm s-1 for 30 min
(He and Wardle, 1988
). Sockeye
salmon (18.5 cm) maintained a speed of 77.4 cm s-1 for 60 min at 15
°C but only 69.4 cm s-1 for 60 min at 24 °C
(Brett and Glass, 1973
). On the
basis of the speed at which the fast, glycolytic muscle fibers are first
recruited, as determined from electromyographic recordings, the
Umax,c at 24 °C for 18.48±0.32 cm striped bass
was 2.82±0.32 body lengths s-1 or approximately 52 cm
s-1 (Sisson and Sidell,
1987
), and the Umax,c at 20 °C for 20-25
cm scup was 80-81 cm s-1 (Rome
et al., 1992
; Swank and Rome,
2000
). Only the values for the striped bass and the sockeye salmon
at 24 °C are lower than comparable values for S. japonicus from
the present study.
The fact that the chub mackerel can achieve a higher
Umax,c at 24 than at 18 °C is probably due to greater
muscle fiber contraction rate and power output at the higher temperature, as
has been found in isolated slow, oxidative muscle fibers of other scombrids
(Johnston and Brill, 1984;
Altringham and Block, 1997
) and
other teleosts (e.g. Rome and Swank,
1992
; Rome et al.,
2000
). Because of the effect of temperature on power output, the
lower the temperature, the lower the speed at which the fast, glycolytic
muscle fibers are first recruited and, thus, the lower the
Umax,c, since that is the maximum speed powered only by
the aerobic muscle fibers. This is the `compression of recruitment order
theory' of Rome et al. (1984
)
(see also Sisson and Sidell,
1987
; Rome, 1990
,
1995
). However, if more slow,
oxidative muscle fibers are contracting at a given speed at 18 than at 24
°C, COTnet would be expected to be higher at 18 °C, not
lower.
The total energetic cost (VO2) at each speed was higher
at 24 than at 18 °C, and the difference between the two planes along the
y-axis in Fig. 3
represents the magnitude of the effect of temperature on a combination of
locomotor and support costs. This difference was not affected by fish mass but
did increase with swimming speed at the higher temperature, as indicated by
steeper slopes for the O2
versus speed regressions (i.e. the COTnet values). The
higher COTnet may be a consequence of the fact that mackerel
reached higher speeds at 24 than at 18 °C, since the amount of muscle
contractile power required to swim should increase exponentially with speed.
However, if the data points for the higher speeds (
100 cm s-1)
at 24 °C are excluded, the slopes of the
O2 versus speed
regressions decrease somewhat, but are still greater at 24 than at 18 °C,
suggesting that other factors contribute to this difference.
The O2 at each speed
could be higher at 24 °C because of higher swimming support costs, such as
a higher cardiac output and blood flow to the slow, oxidative locomotor muscle
to compensate for the lower O2 solubility at the higher
temperature. Other energetic expenditures, such as those for ion regulation
and osmoregulation, could also be higher at the higher temperature. In
addition, the mackerel at 24 °C may have been more stressed than those at
18 °C, or post-feeding specific dynamic action may have contributed more
to
O2 at 24 °C because
of the different lengths of the initial adjustment period in the respirometer
(4 h for the 24 °C-acclimated mackerel versus 12-19 h for the 18
°C-acclimated mackerel). Unfortunately, we were unable to quantify any of
these costs or to separate the effects of temperature on the direct costs of
swimming (production of propulsive force by myotomal muscle) from these other
potential energetic demands.
There are other possible reasons why total
O2 and
COTnet are greater at the higher temperature. First, slow,
oxidative muscle fiber contraction at a given speed could be less efficient at
24 than at 18 °C in the chub mackerel. There are few studies of muscle
fiber contraction efficiency in fishes, and none that we know of that has
investigated the effect of temperature. In individual human slow, oxidative
muscle fibers, the thermodynamic efficiency of contraction increased with an
increase in temperature (He et al.,
2000
). In frog muscle, there was little change in the mechanical
efficiency of contraction with temperature
(Rall and Woledge, 1990
), and
we could find no studies of vertebrate skeletal muscle showing a decrease in
efficiency with an increase in temperature. Nevertheless, in the mackerel in
the present study, a change in muscle fiber characteristics leading to an
increase in efficiency could have occurred during the acclimation period at 18
°C, as suggested for scup by Swank and Rome
(2001
). In other teleosts
acclimated to low temperatures, the amount of slow, oxidative myotomal muscle
increased [e.g. in carp (Sidell,
1980
), striped bass (Jones and
Sidell, 1982
) and rainbow trout
(Taylor et al., 1996
)], and
cyprinid fishes can alter their muscle contractile properties to compensate
for low temperature (for reviews, see
Sidell and Moerland, 1989
;
Rome, 1995
), as can scup
(Swank and Rome, 2001
).
However, we did not measure any of these variables, so we cannot determine
whether any temperature-compensatory adjustments occurred.
Second, at a given speed and tail-beat frequency, the slow, oxidative
muscle fibers could be operating at a different point on the force/velocity or
power output/stimulation frequency curves at the two temperatures
(Stevens, 1979;
Sisson and Sidell, 1987
;
Rome, 1995
). In isolated slow,
oxidative muscle of the eastern Pacific bonito Sarda chiliensis, an
ectothermic scombrid species, and the yellowfin tuna Thunnus
albacares, Altringham and Block
(1997
) found an increase with
temperature in the frequency at which maximum power was generated. Thus, in
the chub mackerel, a given tail-beat frequency could be closer to the optimal
stimulation frequency at 18 than at 24 °C. However, since maximum power
output also increases with temperature, more power can be produced by
stimulating the muscle fibers at 24 °C at a sub-optimal frequency than by
stimulating the muscle fibers at 18 °C at their optimal frequency.
Furthermore, Rome and colleagues found that, even though acclimation to 10
°C, improved power output at 10 °C, scup produced less power from
their slow, oxidative muscle at 10 °C than they could at 20 °C
(Rome et al., 2000
;
Rome and Swank, 2001
; Swank
and Rome, 2000
,
2001
). To understand slow,
oxidative muscle function at the different temperatures in chub mackerel, it
will be necessary to combine in vivo measurements of muscle
stimulation pattern and muscle strain along the length of the fish with in
vitro work loop studies, as a function of temperature.
Third, Sisson and Sidell
(1987) suggested that an
increase in water kinematic viscosity at a lower temperature could delay
boundary layer separation, thus reducing drag and the energetic cost of
swimming at a given speed at the lower temperature. Although not tested in the
present study, others have shown that changes in water kinematic viscosity
contribute little to temperature effects on fish swimming performance for the
size of fish swimming at the speeds used here; significant effects of water
viscosity have been demonstrated only with fish larvae and small juveniles at
relatively low speeds, i.e. at low Reynolds numbers
(Fuiman and Batty, 1997
;
Johnson et al., 1998
).
However, in the water flow regimes associated with swimming tunnels, boundary
layer effects may become important. With new methods of visualizing and
quantifying flow within the boundary layer of swimming fish
(Anderson et al., 2001
), the
hypothesized effects of water temperature and kinematic viscosity on boundary
layer separation could be explored.
Swimming kinematics
At both 18 and 24 °C, there were significant effects of swimming speed
and fish size on tail-beat frequency, tail-beat amplitude and stride length,
as expected on the basis of a number of other studies of swimming kinematics
in fishes (for a review, see Donley and
Dickson, 2000). The data for tail-beat frequency versus
speed in the present study are similar to those reported previously for S.
japonicus (26.3-32.2 cm FL) at 17.0-19.5 °C by Hunter and
Zweifel (1971
).
At a given speed and fish size, there were no significant effects of
temperature on tail-beat frequency, tail-beat amplitude or stride length. This
is consistent with several previous investigations with other teleost fishes
in which tail-beat frequency and/or tail-beat amplitude at a given speed were
not affected by temperature (Smit et al.,
1974; Rome and Sosnicki,
1990
; Rome et al.,
1990
,
1992
). However, in other
studies (Stevens, 1979
;
Sisson and Sidell, 1987
), the
tail-beat frequency at a given speed did vary with temperature, which was
attributed to higher thrust per tail beat, greater propeller efficiency and/or
lower drag at the lower temperatures. In those studies, fish were acclimated
to and/or measured at temperatures representing a wider range than was used in
the present study.
The only kinematic variable that was significantly affected by temperature
in the chub mackerel was propulsive wavelength, which also increased
significantly with FL, as expected, but not with fish mass or
swimming speed. The increase in (=propulsive wave velocity/tail-beat
frequency) with temperature is due to a higher propulsive wave velocity at 24
°C because tail-beat frequency was not significantly affected by
temperature. It is not clear why
, but none of the other kinematic
variables measured, would vary with temperature. A faster propulsive wave
velocity at 24 °C could result if temperature enhanced the rate at which
action potentials within the motor neurons and muscle fibers propagated
posteriorly down the fish or if the latent period between electrical
activation and muscle contraction decreased. However, in scup acclimated to
and studied at both 10 and 20 °C, there was no significant effect of
temperature on the speed at which electrical activity (measured by
electromyography) moved posteriorly along the body or on propulsive wave
velocity (Rome and Swank,
2001
).
A higher at the higher temperature could result from an increase
in flexural stiffness (Long et al.,
1994
; McHenry et al.,
1995
; Long and Nipper,
1996
). Stiffness could be increased if the active muscles were to
do more negative work at 24 than at 18 °C
(McHenry et al., 1995
;
Long and Nipper, 1996
), but
there is no evidence of net negative work being produced by slow, oxidative
muscle contraction in swimming chub mackerel
(Shadwick et al., 1998
).
Furthermore, on the basis of work loop studies with isolated slow, oxidative
muscle of other teleosts, including two scombrid species
(Altringham and Block, 1997
;
Rome et al., 2000
;
Rome and Swank, 2001
; Swank
and Rome, 2000
,
2001
), more net positive work
should be produced at the higher temperature. It should also be noted that
there is considerable overlap in the propulsive wavelength data at the two
temperatures in the present study (Fig.
8).
Relevance to endothermy in tunas
The positive effect of temperature on whole-animal swimming performance
(Umax,c) measured in the present study is very similar in
magnitude to the effect of temperature on contraction rate and power output in
isolated slow oxidative myotomal muscle fibers of the two scombrid fishes
studied by Altringham and Block
(1997).
Umax,c values in the chub mackerel increased by
approximately 30 % with an increase of 6 °C compared with a 22-37 %
increase in maximal power output between 20 and 25 °C in the isolated
scombrid muscle fibers. This suggests that results of such in vitro
experiments may be used to estimate the effects of temperature on sustainable
swimming speeds of fish; however, one must consider the precautions for doing
so discussed by Rome (1995
)
and Rome et al. (2000
). If the
power output of slow, oxidative myotomal muscle in tunas is enhanced at higher
temperatures in vivo, as was found by Altringham and Block
(1997
) in vitro, then
increased maximal sustainable swimming speeds should result from the
maintenance of elevated myotomal muscle temperatures in tunas. This hypothesis
needs to be tested by comparing the maximal sustainable swimming speed of
larger tunas, in which Tm is elevated more than a few
degrees above the water temperature, with that of similar-sized ectothermic
scombrid fishes (preferably a bonito, one of the tunas' sister group) at the
same water temperature. Because this has not yet been accomplished, there has
been no unequivocal test of the hypothesis that endothermy enhances
sustainable swimming performance in tunas (see
Sepulveda and Dickson, 2000
).
The present study, by measuring the effects of temperature on an ectothermic
species that is closely related to the tunas, provides evidence that
maintaining Tm
6 °C above the ambient water
temperature may significantly increase sustainable swimming speeds in tunas.
The present study also suggests that the tunas would incur a higher
COTnet.
However, there is an important difference between a tuna swimming in
18°C water with its slow, oxidative locomotor muscle maintained at
24°C and a mackerel at 24°C. In the tuna, the heart temperature would
be approximately 18°C. Because heart rate decreases with decreasing
temperature in tunas (Korsmeyer et al.,
1997), cardiac output will be reduced, and perfusion of the slow,
oxidative muscle fibers may also be reduced. If the rate of perfusion is not
sufficient to maintain aerobic function within these muscle fibers at high
contraction rates, the maximum sustainable swimming speed would be lower than
that predicted on the basis of the elevated slow, oxidative muscle
temperature. In fact, on the basis of swimming behavior in relation to water
temperature, Brill et al.
(1999
) have hypothesized that
the effects of temperature on cardiac function limit the thermal range of at
least some tuna species. However, the higher heart mass, cardiac output,
hemoglobin concentration and muscle myoglobin content of tunas compared with
ectothermic scombrids and other active teleosts (for reviews, see Dickson,
1995
,
1996
;
Brill and Bushnell, 2001
) may
allow the slow, oxidative locomotor muscle to maintain maximal function at its
high temperature, despite being supplied by a cooler heart. Additional work is
needed to understand fully how locomotor muscle physiology and cardiac
function are integrated in tunas in vivo.
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Acknowledgments |
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References |
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