MYOTOMAL MUSCLE FUNCTION AT DIFFERENT LOCATIONS IN THE BODY OF A SWIMMING FISH

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.

1994 ◽  
Vol 267 (2) ◽  
pp. R481-R488 ◽  
Author(s):  
T. P. Johnson ◽  
D. A. Syme ◽  
B. C. Jayne ◽  
G. V. Lauder ◽  
A. F. Bennett

We recorded electromyograms of slow-twitch (red) muscle fibers and videotaped swimming in the largemouth bass (Micropterus salmoides) during cruise, burst-and-glide, and C-start maneuvers. By use of in vivo patterns of stimulation and estimates of strain, in vitro power output was measured at 20 degrees C with the oscillatory work loop technique on slow-twitch fiber bundles from the midbody area near the soft dorsal fin. Power output increased slightly with cycle frequency to a plateau of approximately 10 W/kg at 3-5 Hz, encompassing the normal range of tail-beat frequencies for steady swimming (approximately 2-4 Hz). Power output declined at cycle frequencies simulating unsteady swimming (burst-and-glide, 10 Hz; C-start, 15 Hz). However, activating the muscle at 10 Hz did significantly increase the net work done compared with the work produced by the inactive muscle (work done by the viscous and elastic components). Thus this study provides further insight into the apparently paradoxical observation that red muscle can contribute little or no power and yet continues to show some recruitment during unsteady swimming. Comparison with published values of power requirements from oxygen consumption measurements indicates a limit to steady swimming speed imposed by the maximum power available from red muscle.


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.


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.


2001 ◽  
Vol 204 (13) ◽  
pp. 2231-2238 ◽  
Author(s):  
D. J. Ellerby ◽  
I. L. Y. Spierts ◽  
J. D. Altringham

SUMMARYEels are capable of locomotion both in water and on land using undulations of the body axis. Axial undulations are powered by the lateral musculature. Differences in kinematics and the underlying patterns of fast muscle activation are apparent between locomotion in these two environments. The change in isometric fast muscle properties with axial location was less marked than in most other species. Time from stimulus to peak force (Ta) did not change significantly with axial position and was 82±6ms at 0.45BL and 93±3ms at 0.75BL, where BL is total body length. Time from stimulus to 90% relaxation (T90) changed significantly with axial location, increasing from 203±11ms at 0.45BL to 239±9ms at 0.75BL. Fast muscle power outputs were measured using the work loop technique. Maximum power outputs at ±5% strain using optimal stimuli were 17.3±1.3Wkg−1 in muscle from 0.45BL and 16.3±1.5Wkg−1 in muscle from 0.75BL. Power output peaked at a cycle frequency of 2Hz. The stimulus patterns associated with swimming generated greater force and power than those associated with terrestrial crawling. This decrease in muscle performance in eels may occur because on land the eel is constrained to a particular kinematic pattern in order to produce thrust against an underlying substratum.


1999 ◽  
Vol 202 (23) ◽  
pp. 3397-3403 ◽  
Author(s):  
J.D. Altringham ◽  
D.J. Ellerby

Undulatory swimming in fish is powered by the segmental body musculature of the myotomes. Power generated by this muscle and the interactions between the fish and the water generate a backward-travelling wave of lateral displacement of the body and caudal fin. The body and tail push against the water, generating forward thrust. The muscle activation and strain patterns that underlie body bending and thrust generation have been described for a number of species and show considerable variation. This suggests that muscle function may also vary among species. This variation must be due in large part to the complex interactions between muscle mechanical properties, fish body form, swimming mode, swimming speed and phylogenetic relationships. Recent work in several laboratories has been directed at studying patterns of muscle power output in vitro under simulated swimming conditions. This work suggests that the way that fish generate muscle power and convert it into thrust through the body and caudal fin does indeed vary. However, despite the differences, several features appear to be common to virtually all species studied and suggest where future effort should be directed if muscle function in swimming fish is to be better understood.


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


1989 ◽  
Vol 142 (1) ◽  
pp. 17-29 ◽  
Author(s):  
C. J. PENNYCUICK ◽  
M. R. FULLER ◽  
LYNNE McALLISTER

Two Harris' hawks were trained to fly along horizontal and climbing flight paths, while carrying loads of various masses, to provide data for estimating available muscle power during short flights. The body mass of both hawks was about 920 g, and they were able to carry loads up to 630 g in horizontal flight. The rate of climb decreased with increasing all-up mass, as also did the climbing power (product of weight and rate of climb). Various assumptions about the aerodynamic power in low-speed climbs led to estimates of the maximum power output of the flight muscles ranging from 41 to 46 W. This, in turn, would imply a stress during shortening of around 210 kPa. The effects of a radio package on a bird that is raising young should be considered in relation to the food load that the forager can normally carry, rather than in relation to its body mass.


1998 ◽  
Vol 201 (10) ◽  
pp. 1659-1671 ◽  
Author(s):  
L Hammond ◽  
J D Altringham ◽  
C S Wardle

Strain and activity patterns were determined during slow steady swimming (tailbeat frequency 1.5-2.5 Hz) at three locations on the body in the slow myotomal muscle of rainbow trout Oncorhynchus mykiss using sonomicrometry and electromyography. Strain was independent of tailbeat frequency over the range studied and increased significantly from +/-3.3 % l0 at 0.35BL to +/-6 % at 0.65BL, where l0 is muscle resting length and BL is total body length. Muscle activation occurred significantly later in the strain cycle at 0.35BL (phase shift 59 degrees) than at 0.65BL (30 degrees), and the duration of activity was significantly longer (211 degrees at 0.35BL and 181 degrees at 0.65BL). These results differ from those of previous studies. The results have been used to simulate in vivo activity in isolated muscle preparations using the work loop technique. Preparations from all three locations generated net positive power under in vivo conditions, but the negative power component increased from head to tail. Both kinematically, and in the way its muscle functions to generate hydrodynamic thrust, the rainbow trout appears to be intermediate between anguilliform swimmers such as the eel, which generate thrust along their entire body length, and carangiform fish (e.g. saithe Pollachius virens), which generate thrust primarily at the tail blade.


2020 ◽  
Vol 223 (21) ◽  
pp. jeb225839 ◽  
Author(s):  
Joseph W. Bahlman ◽  
Vikram B. Baliga ◽  
Douglas L. Altshuler

ABSTRACTBirds that use high flapping frequencies can modulate aerodynamic force by varying wing velocity, which is primarily a function of stroke amplitude and wingbeat frequency. Previous measurements from zebra finches (Taeniopygia guttata) flying across a range of speeds in a wind tunnel demonstrate that although the birds modulated both wingbeat kinematic parameters, they exhibited greater changes in stroke amplitude. These two kinematic parameters contribute equally to aerodynamic force, so the preference for modulating amplitude over frequency may instead derive from limitations of muscle physiology at high frequency. We tested this hypothesis by developing a novel in situ work loop approach to measure muscle force and power output from the whole pectoralis major of zebra finches. This method allowed for multiple measurements over several hours without significant degradation in muscle power. We explored the parameter space of stimulus, strain amplitude and cycle frequencies measured previously from zebra finches, which revealed overall high net power output of the muscle, despite substantial levels of counter-productive power during muscle lengthening. We directly compared how changes to muscle shortening velocity via strain amplitude and cycle frequency affected muscle power. Increases in strain amplitude led to increased power output during shortening with little to no change in power output during lengthening. In contrast, increases in cycle frequency did not lead to increased power during shortening but instead increased counter-productive power during lengthening. These results demonstrate why at high wingbeat frequency, increasing wing stroke amplitude could be a more effective mechanism to cope with increased aerodynamic demands.


2007 ◽  
Vol 362 (1487) ◽  
pp. 1995-2016 ◽  
Author(s):  
Lawrence C Rome

There is a significant reduction in overall maximum power output of muscle at low temperatures due to reduced steady-state (i.e. maximum activation) power-generating capabilities of muscle. However, during cyclical locomotion, a further reduction in power is due to the interplay between non-steady-state contractile properties of muscle (i.e. rates of activation and relaxation) and the stimulation and the length-change pattern muscle undergoes in vivo . In particular, even though the relaxation rate of scup red muscle is slowed greatly at cold temperatures (10°C), warm-acclimated scup swim with the same stimulus duty cycles at cold as they do at warm temperature, not affording slow-relaxing muscle any additional time to relax. Hence, at 10°C, red muscle generates extremely low or negative work in most parts of the body, at all but the slowest swimming speeds. Do scup shorten their stimulation duration and increase muscle relaxation rate during cold acclimation? At 10°C, electromyography (EMG) duty cycles were 18% shorter in cold-acclimated scup than in warm-acclimated scup. But contrary to the expectations, the red muscle did not have a faster relaxation rate, rather, cold-acclimated muscle had an approximately 50% faster activation rate. By driving cold- and warm-acclimated muscle through cold- and warm-acclimated conditions, we found a very large increase in red muscle power during swimming at 10°C. As expected, reducing stimulation duration markedly increased power output. However, the increased rate of activation alone produced an even greater effect. Hence, to fully understand thermal acclimation, it is necessary to examine the whole system under realistic physiological conditions.


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