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First published online March 16, 2007
Journal of Experimental Biology 210, 1194-1203 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02730
Thermal dependence of contractile properties of the aerobic locomotor muscle in the leopard shark and shortfin mako shark
1 Biology Department, MiraCosta College, Oceanside, CA 92056, USA
2 Marine Biology Research Division, Scripps Institution of Oceanography
University of California, San Diego, La Jolla, CA 92093-0202, USA
3 Pfleger Institute of Environmental Research, Oceanside, CA 92054,
USA
4 Department of Biological Sciences, University of Calgary, Calgary,
Alberta, T2N 1N4, Canada
* Author for correspondence at present address: Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada (e-mail: shadwick{at}zoology.ubc.ca)
Accepted 23 January 2007
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Key words: red muscle, temperature, contractile properties, work loop, lamnid, Isurus, Triakis
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;
Donley et al., 2005). This is
in contrast to most bony fishes, in which decreases in duty cycle and advances
in the phase of onset of RM activation relative to the muscle strain cycle
typically occur from anterior to posterior
(Altringham and Ellerby, 1999;
Gillis, 1998;
Coughlin, 2002). Since changes
in activation timing can have a significant effect on the net work and power
produced by a muscle [e.g. scup Stenotomus chrysops
(Rome et al., 1993); saithe
Pollachius virens white muscle
(Altringham et al., 1993);
rainbow trout Oncorhynchus mykiss
(Hammond et al., 1998);
largemouth bass Micropterus salmoides
(Coughlin, 2000)], many
studies on bony fishes have concluded that the longitudinal phase shift in
activation timing leads to regional variation in muscle function (for reviews,
see Altringham and Ellerby,
1999; Coughlin,
2000) which may be important in undulatory swimming. The lack of
such changes in sharks, including the undulatory leopard shark, might suggest
a divergent reliance on force and power for swimming.
A number of physiological properties of muscle will influence power output,
including activation kinetics, force–velocity characteristics, and the
relative timing of onset and offset of activation during movement.
(Josephson, 1999). A key
difference between mako and leopard sharks swimming in 20°C water is that
the phases of onset and offset of RM activation are approximately 30°
later in the strain cycle in the mako
(Donley et al., 2005). This
later activation phase predicts several potential differences in muscle
function. First, it suggests that RM in the mako may be faster, allowing it to
develop force and relax faster than the leopard shark. Thus, mako RM may
absorb proportionally less lengthening work and produce more net positive work
in each contraction cycle. Second, shorter activation and relaxation times
allow muscle to operate at higher cycle frequencies, so the mako may have a
greater range of aerobic swimming speeds than the leopard shark. Third, due to
the relatively late activation of RM in the mako, there is virtually no period
during which posterior fibers perform lengthening work (i.e. active while
being lengthened). In the leopard shark, by contrast, active lengthening of
the mid- and posterior muscle coincides with active shortening in the anterior
for about 10% of each tailbeat cycle
(Donley and Shadwick, 2003).
During this time the posterior fibers may develop high force and act to
stiffen the body, facilitating power transmission from the anterior muscle
along the body to the tail, as has been hypothesized for some teleosts
(Altringham et al., 1993).
Transmission of force in the mako may simply rely on tendons rather than on
transient properties of the posterior musculature
(Donley et al., 2004).
This study examines whether muscle function is indeed constant along the body in elasmobranchs by testing the hypothesis that the power production and contractile properties of the red, aerobic, locomotor muscles do not vary longitudinally in the leopard shark and shortfin mako. Furthermore, we identify potential differences in the contractile properties between ecto- and endothermic sharks, including the effects of temperature on optimal stimulus duration, phase, net work and power output. Based on later EMG onset and offset times measured in swimming mako sharks mentioned above, it is hypothesized that red muscle from mako sharks will produce power at greater cycle frequencies than the red muscle of leopard sharks, at a given temperature.
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). At SIO, the leopard sharks were maintained in a 3-m
diameter tank with continuous flow of seawater and aeration for several weeks
prior to experimentation at a water temperature that reflected the ambient
coastal conditions (15–20°C). These sharks were fed squid and
chopped fish weekly until satiation. Because to date mako sharks cannot be
maintained in aquaria for prolonged periods, the muscle tissue samples were
taken from each test specimen immediately upon arrival at SIO. All procedures
in capture, maintenance and experimentation followed the guidelines of our
University of California, San Diego animal care protocol.
Muscle preparation
Animals were killed by severing of the spinal cord. Small blocks of red
muscle (RM) were collected from two axial positions (0.4 L anterior
and 0.6–0.65 L posterior) and immediately placed into chilled
(5–10°C), oxygenated elasmobranch saline (composition in mmol
l–1: NaCl, 292; KCl, 3.2; CaCl2, 5.0;
MgSO4, 1.0; Na2SO4, 1.6; NaHCO3,
5.9; TMAO, 150; Urea, 300; Glucose, 10; pH 7.8 at 20°C). The muscle blocks
were then dissected to isolate small bundles spanning a single myomere
(
0.5 mm in diameter). The preparations were rinsed with chilled
oxygenated saline frequently during dissection. Bundles were then transferred
to a temperature-controlled chamber filled with circulating oxygenated saline.
Braided silk (5-0) surgical suture was used to attach the collagenous myosepta
on the ends of each muscle bundle to the force transducer (Grass model FTO3C;
Quincy, MA, USA) and the servomotor lever arm (model 305B-LC, Aurora
Scientific, Aurora, Ontario, Canada).
Assessment of contractile properties
Once each bundle was attached to the force transducer and servomotor lever
arm, the preparation was stretched to remove visible slack. A pair of
platinum-tipped stimulating electrodes was positioned next to the muscle and
the voltage adjusted to 150% of that required to produce maximum, isometric
twitch force. A force–length curve was then constructed by stimulating
the muscle preparation with short duration (1 ms) stimuli and measuring
isometric twitch force over a range of muscle lengths. The length of the
bundle was adjusted by increments of 2–5%L between each
stimulus. The peak in the force–length curve was not always distinct, so
the criteria for establishing optimal length were that at which developed
force was at or near maximal while passive tension just began to rise. The
minimum stimulus frequency that produced maximum, isometric, tetanic force was
about 60 Hz at all experimental temperatures (15–28°C) and was used
in all experiments. The stimulus duration required to elicit maximum,
isometric, tetanic force was typically 600 ms. Isometric tetanic force was
recorded routinely throughout the experiments to monitor stability of the
preparation, and remained stable in all preparations, declining by no more
than 5%.
To measure mechanical work and power output
(Josephson, 1985;
Josephson, 1993), each muscle
bundle was subjected to a series of sinusoidal length changes centered about
the optimal length and stimulated to contract under conditions of strain (%
length change) recorded in vivo [±4.0% for the anterior and
±6.0% for the posterior muscle in the leopard shark; ±5.5%
anterior and ±9.0% posterior muscle in the mako
(Donley and Shadwick, 2003;
Donley et al., 2004)]. Work
loop experiments were performed over a series of cycle frequencies ranging
from 0.25 to 3 Hz, encompassing the range over which the RM could produce
substantial net positive work. At each combination of strain and cycle
frequency, stimulus duration and phase were adjusted in increments of 25
ms and 5–10°, respectively, until net work production was maximal,
requiring up to 10 work loops for each cycle frequency. Stimulus phase,
defined as the point in the strain cycle when the stimulus begins, is
expressed in degrees of the sinusoidal length change cycle ranging from 0°
to 360°, where 0° is mean length during the lengthening portion of the
cycle and 90° is peak muscle length. Stimulus duration is the period of
muscle activation. Stimulus phase, duration, the amplitude of length change,
and cycle frequency were controlled using custom software written in Labview
(National Instruments, Austin, TX, USA). Net work of each complete strain
cycle was calculated as the integral of force with respect to length. Power
output was calculated as the product of work per cycle and cycle
frequency.
The effects of temperature on twitch kinetics, work and power were also
examined. Temperatures encompass those normally experienced in the water by
both the leopard and mako sharks, typically ranging from 14 to 20°C
(Cailliet, 1992;
Sepulveda et al., 2004).
Because the leopard shark is ectothermic, its body (and superficial RM)
temperature conforms to that of the surrounding environment and thus normally
fluctuates within this range. For each axial position examined in the leopard
shark we present data from seven RM bundles (from five sharks) measured at 15,
20 and 25±1°C. The mako, like other lamnid sharks, is regionally
endothermic. In free-swimming makos, the temperature of the deep RM has been
shown to be maintained up to 8°C above ambient
(Carey and Teal, 1969;
Carey et al., 1971). So despite
cooler ambient conditions, mako RM may typically fluctuate between 20 and
28°C. For the mako, we present data from nine RM bundles (from seven
sharks) from the anterior position and eight RM bundles from the posterior
position measured at 15, 20 and 28±1°C. The sequence of
temperatures was varied between experiments and all work loop experiments were
repeated at each temperature to quantify any changes in the force production
capacity over the course of the experiment.
Values represent the mean ± standard error (s.e.m.). To avoid errors
associated with estimating viable muscle mass in the preparations, and because
an assessment of absolute work output was not required for the goals of this
study, net work and power output are presented as a percentage of the maximum
values recorded over the range of frequencies for each preparation
(Syme and Shadwick, 2002).
Anterior vs posterior twitch times, activation phase and duration,
and the cycle frequency at which power was maximal, were compared using
t-tests.
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Net work and power output
There was no significant longitudinal variation in the cycle frequencies
producing maximum net work or power output at any temperature in RM from
leopard or mako sharks (P>0.05). Therefore, as with stimulation
parameters, data for anterior and posterior work and power output were pooled
and normalized (Fig. 6). In the
case of net work, data are expressed as a percentage of the maximum work
recorded at each temperature to emphasize the sensitivity of work to cycle
frequency at different temperatures in the two sharks. The cycle frequency
producing maximum net work was nearly invariant with temperature in the
leopard shark (at about 0.5 Hz), but increased from 0.25 Hz at 15°C to 1.0
Hz at 28°C in the mako (Fig.
6A,B). Power output for all temperatures is expressed as a
percentage of the maximum power recorded at 20°C to highlight the
differences in temperature sensitivity of power in the two species
(Fig. 6C,D). Power output was
relatively high at low temperatures but reduced at high temperature in the
leopard shark, whereas power was relatively poor at low temperature and high
at high temperatures in the mako. Muscle power output in the mako was greatest
at 28°C, reaching 120% of the peak at 20°C and remaining above 80% up
to at least 3 Hz. Even at 20°C, where the pattern of power output was most
similar between the leopard and mako sharks, power output stayed elevated in
the mako shark (>60% of peak) up to 2 Hz, while declining in the leopard
shark to about 25% of peak at 2 Hz. Leopard shark RM showed only a small
increase in the cycle frequency for maximum power output when temperature
increased from 15 to 25°C (Fig.
6C, Fig. 7). In
mako shark RM the frequency for maximum power increased markedly with
temperature over the entire range studied, from 0.25 Hz at 15°C to >2
Hz at 28°C (Fig. 6D,
Fig. 7).
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Contractile properties do not vary longitudinally
Longitudinal variation in RM function is common, although not ubiquitous,
among bony fishes (Gillis,
1998; Altringham and Ellerby,
1999; Coughlin,
2002). Studies have shown differences in patterns of power
production and variation in isometric twitch kinetics along the body in
several species of bony fish. Slower rates of relaxation [scup S.
chrysops (Coughlin et al.,
1996); yellowfin tuna T. albacares
(Altringham and Block, 1997);
largemouth bass M. salmoides
(Coughlin, 2000)] and slower
rates of activation in the posterior musculature relative to the anterior
[rainbow trout O. mykiss (Hammond
et al., 1998; Coughlin et al.,
2001) have been documented. In contrast, the current study noted
no significant differences in the twitch kinetics between anterior and
posterior RM in leopard sharks from 15–25°C, or in mako sharks from
20–28°C (Figs 1,
2). Furthermore, in both
species there were no significant differences in optimal stimulus duration or
phase for work from RM at the two axial positions
(Fig. 5). Consequently,
patterns of work and power production as a function of cycle frequency were
similar in the anterior and posterior positions for both shark species
(Fig. 6). These observations
and the consistency in activation duty cycle and phase recorded along the body
during steady swimming (Donley and
Shadwick, 2003; Donley et al.,
2005) all support the hypothesis that contractile properties and
thus muscle function is constant along the body in the leopard and mako sharks
(at least within the normal physiological temperature range).
Our findings lead us to conclude that longitudinal variation in contractile
performance of muscle may occur only in bony fishes; at this point, there is
no evidence to the contrary. Perhaps sharks utilize a lower diversity of
locomotor behaviors and thus may not require such differential muscle function
along the body. Despite an apparent lack of difference in axial performance,
there is an increase in red muscle strain from anterior to posterior in both
sharks during steady swimming [4% vs 6% leopard, 5.5% vs 9%
mako (Donley and Shadwick,
2003; Donley et al.,
2005)], a characteristic likely to increase total power output
during cyclical contractions (Altringham
and Johnston, 1990; Syme and
Shadwick, 2002). In addition to increased strain, muscle fiber
length increases dramatically along the body in both species (J.M.D.,
unpublished data) and therefore larger absolute length changes occur in the
posterior muscle fibres. Therefore, these sharks may produce greater power
output in the posterior due to a combination of greater fiber lengths and
strains even though the muscle contractile properties are constant.
Temperature effects
Temperature has a significant effect on power output of fish muscle (see
Syme, 2006). To accommodate
swimming at low temperatures, fish may decrease stimulus duration (duty
cycle), decrease activation phase so that muscle is activated earlier in its
strain cycle, recruit more muscle fibers, or simply swim at a slower tailbeat
frequency (Swank and Rome,
1999). Temperature modulated increases in muscle power output are
also common in teleosts fishes: e.g. sculpin Myoxocephalus scorpius
WM (Johnson and Johnston,
1991); scup RM (Rome and
Swank, 1992); tuna and bonito RM
(Altringham and Block,
1997).
Optimal activation of RM from the ectothermic leopard shark required only a small decrease in the duty cycle, from 35% to 20% of a cycle, between 25 and 15°C, while the most significant temperature effect was on the RM of the endothermic mako, particularly at the lowest temperature, where the duty cycle decreased from about 40% down to 10% or less, when cooled from 28°C to 15°C. Stimulus phase for maximum work was largely insensitive to temperature changes, particularly in the leopard shark, although a trend to lower phases with decreasing temperature was observed, as would be expected from the concomitant slowing of twitch kinetics.
There was a much greater effect of temperature on work and power output of red muscle in the mako than in the leopard shark (Fig. 6). In the mako, performance was significantly enhanced with temperatures up to 28°C, while in the leopard shark power actually declined slightly at the warm temperature. When cooled to 15°C mako RM bundles did not perform well even when stimulation was optimized at slow frequencies. For example, the net work at 1 Hz was only about 10% of the work generated at 0.25 Hz, and this fell to zero by 1.5 Hz (Fig. 6B). But in the leopard shark power output was not markedly depressed by cool temperature. The poor performance of mako RM at 15°C suggests that this temperature may be below the range in which it can function effectively. In contrast, leopard shark RM showed a broad temperature tolerance with perhaps a lower thermal maximum.
Increases in temperature yielded a much more pronounced increase in the
cycle frequency producing peak RM power output in the mako than in the leopard
shark. If the cycle frequency is considered a proxy for tailbeat frequency,
and therefore swim speed, then the results in
Fig. 7 predict that the mako
may be able to power swimming at greater sustained tailbeat frequencies (and
speeds) than the leopard shark, as long as its RM temperature remains above
about 20°C, but not below. Interestingly, recent experiments on the
endothermic salmon shark Lamna ditropis
(Bernal et al., 2005) showed an
even more pronounced temperature sensitivity in RM, such that power production
was greatly enhanced with temperatures up to at least 30°C but was
virtually zero below 20°C, even though these fish spend much of their time
at water temperatures below 10°C (Weng
et al., 2005). While not so extreme in the mako, it appears that
the RM of endothermic sharks may share this requirement for sustained,
elevated temperatures to function well.
The cycle frequency at which maximum contractile efficiency occurs is
typically slower than that for peak power output
(Curtin and Woledge, 1993a;
Curtin and Woledge, 1993b;
Curtin and Woledge, 1996).
Thus, to ascribe swimming behaviour solely on the basis of the tailbeat
frequencies that produce maximum power could be misleading. It is a reasonable
expectation that fish most frequently cruise at tailbeat frequencies near
optimal for economy (i.e. at the speed of minimum cost of transport)
(Videler, 1993). In the
leopard shark, peak power occurred at relatively slow cycle frequencies
(Fig. 5) that approximate those
commonly observed during free-swimming (0.5–1 Hz)
(Donley and Shadwick, 2003).
This suggests that, for leopard sharks, tailbeat frequencies used most often
may be nearly optimal in terms of both power and efficiency, and that scopes
and range of cruise swimming speeds for maximal power and efficiency are
narrow in a given temperature range. In the mako there was a broad range of
cycle frequencies producing high power at 28°C, with maximum power
occurring above 2.0 Hz. This is at least twice the tailbeat frequency normally
observed in free-swimming mako sharks, and may indicate that in mako sharks
power peaks at greater frequencies than does efficiency
(Sepulveda et al., 2004).
Thus, the mako may be able to sustain greater aerobic swimming speeds at
higher temperatures but at increased metabolic cost.
Onset of RM activation while swimming occurs significantly later in the
strain cycle in the mako than in the leopard shark
(Donley et al., 2005). Based
on this later phase of activation we predicted that mako RM would be faster to
develop force and faster to relax than RM of the leopard shark. Comparison of
the twitch kinetics at each temperature in the two sharks
(Fig. 2) revealed that this was
not the case; if anything the RM of mako sharks is marginally slower, except
at warm temperatures where the two species are similar. The later phase of RM
activation recorded in the mako shark in vivo may simply reflect the
faster twitch kinetics associated with an elevated RM temperature rather than
an intrinsic difference in contractile properties. As stated above, RM
temperatures measured in free-swimming mako sharks are up to 8°C above
that of the ambient water (Carey and Teal,
1969; Carey et al.,
1971). In contrast, the leopard shark, like most sharks, is
ectothermic so its RM temperature matches that of the ambient water.
Therefore, although these two sharks inhabit comparable water temperatures,
their RM may be operating at significantly different temperatures. When the
leopard shark experiences water of 20°C, for example, its RM will produce
maximal power at a tailbeat frequency of 0.75 Hz
(Fig. 7). In the same ambient
conditions, mako RM operates near 28°C and produces maximal power at
>2.0 Hz, affording the mako an advantage in maintaining higher aerobic
swimming speeds.
How do optimal stimulus parameters compare to those predicted from in vivo EMG recordings?
The duration of muscle activation recorded during swimming (i.e. duty
cycle) has been shown to closely match the optimal stimulus duration for
cyclic work in only a few fish species [e.g. in RM of skipjack tuna
(Syme and Shadwick, 2002) and
in RM of scup at warm temperatures (Rome
and Swank, 1992)]. A close agreement was also noted here in both
the leopard and mako sharks. The duration of muscle activation recorded during
swimming was similar at the anterior and posterior axial positions in both the
leopard and mako sharks (Donley and
Shadwick, 2003; Donley et al.,
2005), being roughly 30% of the strain cycle in the leopard shark
and 33% in the mako at a tailbeat frequency of 0.5–1.0 Hz and a water
temperature of 15°C. Given a 30% duty cycle measured in the ectothermic
leopard shark and assuming muscle temperature also to be 15°C, the
stimulus duration would be 600 ms at 0.5 Hz and 300 ms at 1 Hz, which
agrees well with the optimal durations at 15°C
(Fig. 5A). As in some teleosts
(Grillner and Kashin, 1976;
Altringham and Johnston, 1990)
the optimal stimulus duration at all three temperatures in the leopard shark
remained close to a constant proportion of the strain cycle across the range
of cycle frequencies that produced net positive work. Assuming the RM of the
mako shark was operating about 8°C warmer than ambient water temperature
(i.e. near 23°C when in 15°C water), the optimal stimulus durations
for RM of the mako (Fig. 5B at
20–28°C) were again close to the range measured in swimming fish
(33% of the cycle period at 0.5 and 1.0 Hz tailbeat frequency).
Onset of RM activation in leopard sharks swimming at 14–15°C and
tailbeat frequencies of 0.5 to 1.0 Hz typically occurs at 55° of the
strain cycle (Donley and Shadwick,
2003). Mean values for optimal stimulus phase measured in the
present study were only 20–40° at this temperature and tailbeat
frequencies (Fig. 5C). Assuming
the RM of mako sharks is operating near 23°C in 15°C water, the values
for optimal phase (Fig. 5D) are
close to the onset of activation recorded in swimming fish (84°;
swimming at 0.5–1.0 Hz) (Donley
et al., 2005) at 0.5 Hz tailbeat frequency, but not at 1 Hz. At
this time we have no explanation for these discrepancies.
Conclusion
These data support the hypothesis that the contractile properties of RM are
constant along the body in both the leopard and mako sharks, and that the
muscles are used to produce maximal power during swimming under most, but not
all, circumstances. This study also illustrates differences in the effect of
temperature on optimal cycle frequencies for power output in these two sharks.
While these species may experience the same ambient conditions, the RM of mako
sharks operates at significantly higher temperatures than the leopard shark
and maximal power output occurs at a higher cycle frequency in the mako. In
turn the RM of leopard sharks appears to do better at cooler temperatures and
slower cycle frequencies. Ectothermic species like the leopard shark may thus
be able to inhabit cold water but at the expense of a decline in muscle power
output and overall activity. In endothermic sharks like lamnids, the ability
to maintain RM temperatures elevated above that of the ambient water has
perhaps allowed them to expand their thermal niche and exploit waters of a
greater temperature range while maintaining the potential for relatively high
power output and swimming speeds.
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Acknowledgments |
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