Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish.

1997 ◽  
Vol 200 (20) ◽  
pp. 2617-2627 ◽  
Author(s):  
J D Altringham ◽  
B A Block

It has been hypothesised that regional endothermy has evolved in the muscle of some tunas to enhance the locomotory performance of the fish by increasing muscle power output. Using the work loop technique, we have determined the relationship between cycle frequency and power output, over a range of temperatures, in isolated bundles of slow muscle fibres from the endothermic yellowfin tuna (Thunnus albacares) and its ectothermic relative the bonito (Sarda chiliensis). Power output in all preparations was highly temperature-dependent. A counter-current heat exchanger which could maintain a 10 degrees C temperature differential would typically double maximum muscle power output and the frequency at which maximum power is generated (fopt). The deep slow muscle of the tuna was able to operate at higher temperatures than slow muscle from the bonito, but was more sensitive to temperature change than more superficially located slow fibres from both tuna and bonito. This suggests that it has undergone some evolutionary specialisation for operation at higher, but relatively stable, temperatures. fopt of slow muscle was higher than the tailbeat frequency of undisturbed cruising tuna and, together with the high intrinsic power output of the slow muscle mass, suggests that cruising fish have a substantial slow muscle power reserve. This reserve should be sufficient to power significantly higher sustainable swimming speeds, presumably at lower energetic cost than if intrinsically less efficient fast fibres were recruited.

1993 ◽  
Vol 182 (1) ◽  
pp. 191-206 ◽  
Author(s):  
J. D. Altringham ◽  
C. S. Wardle ◽  
C. I. Smith

We describe experiments on isolated, live muscle fibres which simulate their in vivo activity in a swimming saithe (Pollachius virens). Superficial fast muscle fibres isolated from points 0.35, 0.5 and 0.65 body lengths (BL) from the anterior tip had different contractile properties. Twitch contraction time increased from rostral to caudal myotomes and power output (measured by the work loop technique) decreased. Power versus cycle frequency curves of rostral fibres were shifted to higher frequencies relative to those of caudal fibres. In the fish, phase differences between caudally travelling waves of muscle activation and fish bending suggest a change in muscle function along the body. In vitro experiments indicate that in vivo superficial fast fibres of rostral myotomes are operating under conditions that yield maximum power output. Caudal myotomes are active as they are lengthened in vivo and initially operate under conditions which maximise their stiffness, before entering a positive power-generating phase. A description is presented for the generation of thrust at the tail blade by the superficial, fast, lateral muscle. Power generated rostrally is transmitted to the tail by stiffened muscle placed more caudally. A transition zone between power generation and stiffening travels caudally, and all but the most caudal myotomes generate power at some phase of the tailbeat. Rostral power output, caudal force, bending moment and force at the tail blade are all maximal at essentially the same moment in the tailbeat cycle, as the tail blade crosses the swimming track.


1990 ◽  
Vol 148 (1) ◽  
pp. 395-402 ◽  
Author(s):  
JOHN D. ALTRINGHAM ◽  
IAN A. JOHNSTON

Intact, electrically excitable fibre bundles were isolated from the fast and slow myotomal muscle of the bullrout (Myoxocephalus scorpius L.). Power output was measured under conditions simulating their activity in a fish swimming at different speeds. Preparations were subjected to sinusoidal length changes of ±5% of resting length, and stimulated briefly during each cycle. The number and timing of stimuli were adjusted at each cycle frequency to maximise power output. Maximum power was produced at 5–7 Hz for fast fibres (25–35 W kg−1) and 2 Hz for slow fibres (5–8 Wkg−1). Under these conditions, pre-stretch of active muscle provides an important mechanism for storing potential energy for release during the shortening part of the cycle.


2001 ◽  
Vol 204 (7) ◽  
pp. 1369-1379 ◽  
Author(s):  
D.J. Ellerby ◽  
I.L. Spierts ◽  
J.D. Altringham

Eels swim in the anguilliform mode in which the majority of the body axis undulates to generate thrust. For this reason, muscle function has been hypothesised to be relatively uniform along the body axis relative to some other teleosts in which the caudal fin is the main site of thrust production. The European eel (Anguilla anguilla L.) has a complex life cycle involving a lengthy spawning migration. Prior to migration, there is a metamorphosis from a yellow (non-migratory) to a silver (migratory) life-history phase. The work loop technique was used to determine slow muscle power outputs in yellow- and silver-phase eels. Differences in muscle properties and power outputs were apparent between yellow- and silver-phase eels. The mass-specific power output of silver-phase slow muscle was greater than that of yellow-phase slow muscle. Maximum slow muscle power outputs under approximated in vivo conditions were 0.24 W kg(−)(1) in yellow-phase eel and 0.74 W kg(−)(1) in silver-phase eel. Power output peaked at cycle frequencies of 0.3-0.5 Hz in yellow-phase slow muscle and at 0.5-0.8 Hz in silver-phase slow muscle. The time from stimulus offset to 90 % relaxation was significantly greater in yellow- than in silver-phase eels. The time from stimulus onset to peak force was not significantly different between life-history stages or axial locations. Yellow-phase eels shifted to intermittent bursts of higher-frequency tailbeats at a lower swimming speed than silver-phase eels. This may indicate recruitment of fast muscle at low speeds in yellow-phase eels to compensate for a relatively lower slow muscle power output and operating frequency.


2000 ◽  
Vol 203 (2) ◽  
pp. 333-345 ◽  
Author(s):  
L.C. Rome ◽  
D.M. Swank ◽  
D.J. Coughlin

We found previously that scup (Stenotomus chrysops) reduce neither their stimulation duration nor their tail-beat frequency to compensate for the slow relaxation rates of their muscles at low swimming temperatures. To assess the impact of this ‘lack of compensation’ on power generation during swimming, we drove red muscle bundles under their in vivo conditions and measured the resulting power output. Although these in vivo conditions were near the optimal conditions for much of the muscle at 20 degrees C, they were far from optimal at 10 degrees C. Accordingly, in vivo power output was extremely low at 10 degrees C. Although at 30 cm s(−)(1), muscles from all regions of the fish generated positive work, at 40 and 50 cm s(−)(1), only the POST region (70 % total length) generated positive work, and that level was low. This led to a Q(10) of 4–14 in the POST region (depending on swimming speed), and extremely high or indeterminate Q(10) values (if power at 10 degrees C is zero or negative, Q(10) is indeterminate) for the other regions while swimming at 40 or 50 cm s(−)(1). To assess whether errors in measurement of the in vivo conditions could cause artificially reduced power measurements at 10 degrees C, we drove muscle bundles through a series of conditions in which the stimulation duration was shortened and other parameters were made closer to optimal. This sensitivity analysis revealed that the low power output could not be explained by realistic levels of systematic or random error. By integrating the muscle power output over the fish's mass and comparing it with power requirements for swimming, we conclude that, although the fish could swim at 30 cm s(−)(1) with the red muscle alone, it is very unlikely that it could do so at 40 and 50 cm s(−)(1), thus raising the question of how the fish powers swimming at these speeds. By integrating in vivo pink muscle power output along the length of the fish, we obtained the surprising finding that, at 50 cm s(−)(1), the pink muscle (despite having one-third the mass) contributes six times more power to swimming than does the red muscle. Thus, in scup, pink muscle is crucial for powering swimming at low temperatures. This overall analysis shows that Q(10) values determined in experiments on isolated tissue under arbitrarily selected conditions can be very different from Q(10) values in vivo, and therefore that predicting whole-animal performance from these isolated tissue experiments may lead to qualitatively incorrect conclusions. To make a meaningful assessment of the effects of temperature on muscle and locomotory performance, muscle performance must be studied under the conditions at which the muscle operates in vivo.


2012 ◽  
Vol 112 (1) ◽  
pp. 64-71 ◽  
Author(s):  
Jason Tallis ◽  
Rob S. James ◽  
Val M. Cox ◽  
Michael J. Duncan

The ergogenic effects of caffeine in human exercise have been shown to improve endurance and anaerobic exercise performance. Previous work has demonstrated that 70 μM caffeine (physiological maximum) can directly increase mouse extensor digitorum longus (EDL) muscle power output (PO) in sprintlike activity by 3%. Our study used the work loop technique on isolated mouse muscles to investigate whether the direct effect of 70 μM caffeine on PO differed between 1) maximally and submaximally activated muscle; 2) relatively fast (EDL) and relatively slow (soleus) muscles; and 3) caffeine concentrations. Caffeine treatment of 70 μM resulted in significant improvements in PO in maximally and submaximally activated EDL and soleus ( P < 0.03 in all cases). For EDL, the effects of caffeine were greatest when the lowest, submaximal stimulation frequency was used ( P < 0.001). Caffeine treatments of 140, 70, and 50 μM resulted in significant improvements in acute PO for both maximally activated EDL (3%) and soleus (6%) ( P < 0.023 in all cases); however, there was no significant difference in effect between these concentrations ( P > 0.420 in all cases). Therefore, the ergogenic effects of caffeine on PO were higher in muscles with a slower fiber type ( P < 0.001). Treatment with 35 μM caffeine failed to elicit any improvement in PO in either muscle ( P > 0.72 in both cases). Caffeine concentrations below the physiological maximum can directly potentiate skeletal muscle PO. This caffeine-induced increase in force could provide similar benefit across a range of exercise intensities, with greater gains likely in activities powered by slower muscle fiber type.


1994 ◽  
Vol 197 (1) ◽  
pp. 143-164
Author(s):  
D A Syme

Mechanical power and oxygen consumption (VO2) were measured simultaneously from isolated segments of trabecular muscle from the frog (Rana pipiens) ventricle. Power was measured using the work-loop technique, in which bundles of trabeculae were subjected to cyclic, sinusoidal length change and phasic stimulation. VO2 was measured using a polarographic O2 electrode. Both mechanical power and VO2 increased with increasing cycle frequency (0.4-0.9 Hz), with increasing muscle length and with increasing strain (= shortening, range 0-25% of resting length). Net efficiency, defined as the ratio of mechanical power output to the energy equivalent of the increase in VO2 above resting level, was independent of cycle frequency and increased from 8.1 to 13.0% with increasing muscle length, and from 0 to 13% with increasing strain, in the ranges examined. Delta efficiency, defined as the slope of the line relating mechanical power output to the energy equivalent of VO2, was 24-43%, similar to that reported from studies using intact hearts. The cost of increasing power output was greater if power was increased by increasing cycle frequency or muscle length than if it was increased by increasing strain. The results suggest that the observation that pressure-loading is more costly than volume-loading is inherent to these muscle fibres and that frog cardiac muscle is, if anything, less efficient than most skeletal muscles studied thus far.


PLoS ONE ◽  
2017 ◽  
Vol 12 (12) ◽  
pp. e0190335 ◽  
Author(s):  
Axel J. Fenwick ◽  
Alexander M. Wood ◽  
Bertrand C. W. Tanner

1992 ◽  
Vol 170 (1) ◽  
pp. 143-154 ◽  
Author(s):  
M. ELIZABETH ANDERSON ◽  
IAN A. JOHNSTON

Fast muscle fibres were isolated from abdominal myotomes of Atlantic cod (Gadus morhua L.) ranging in size from 10 to 63 cm standard length (Ls). Muscle fibres were subjected to sinusoidal length changes about their resting length (Lf) and stimulated at a selected phase of the strain cycle. The work performed in each oscillatory cycle was calculated from plots of force against muscle length, the area of the resulting loop being net work. Strain and the number and timing of stimuli were adjusted to maximise positive work per cycle over a range of cycle frequencies at 8°C. Force, and hence power output, declined with increasing cycles of oscillation until reaching a steady state around the ninth cycle. The strain required for maximum power output (Wmax) was ±7-11% of Lf in fish shorter than 18 cm standard length, but decreased to ±5 % of Lf in larger fish. The cycle frequency required for Wmax also declined with increasing fish length, scaling to Ls−0.51 under steady-state conditions (cycles 9–12). At the optimum cycle frequency and strain the maximum contraction velocity scaled to Ls−0.79. The maximum stress (Pmax) produced within a cycle was highest in the second cycle, ranging from 51.3 kPa in 10 cm fish to 81.8 kPa in 60 cm fish (Pmax=28.2Ls0.25). Under steady-state conditions the maximum power output per kilogram wet muscle mass was found to range from 27.5 W in a 10 cm Ls cod to 16.4 W in a 60 cm Ls cod, scaling with Ls−0.29 and body mass (Mb)−0.10 Note: To whom reprint requests should be sent


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