The influence of thermal acclimation on power production during swimming. II. Mechanics of scup red muscle under in vivo conditions

2001 ◽  
Vol 204 (3) ◽  
pp. 419-430 ◽  
Author(s):  
D. Swank ◽  
L. Rome
Keyword(s):  
Relaxation Rate ◽  
Cold Acclimation ◽  
Swimming Speed ◽  
Power Output ◽  
Power Production ◽  
Energetic Cost ◽  
Activation Rate ◽  
Seasonal Migrations ◽  
Red Muscle

We have previously shown that the power output of red muscle from warm-acclimated scup is greatly reduced when the fish swim at low temperatures. This reduction occurs primarily because, despite the slowing of muscle relaxation rate at cold temperatures, warm-acclimated scup swim with the same tail-beat frequency and the same stimulation durations, thereby not affording the slower-relaxing muscle any extra time to relax. We hypothesize that power output during swimming could be increased if the stimulus duration were reduced or if the relaxation rate of the red muscle were increased during cold acclimation. Scup were acclimated to 10 degrees C (cold-acclimated) and 20 degrees C (warm-acclimated) for at least 6 weeks. Cold acclimation dramatically increased the ability of scup red muscle to produce power at 10 degrees C. Power output measured from cold-acclimated muscle bundles driven through in vivo conditions measured from cold-acclimated scup swimming at 10 degrees C (i.e. work loops) was generally much greater than that from warm-acclimated muscle driven through its respective in vivo conditions at 10 degrees C. The magnitude of the increase depended both on the anatomical location of the muscle and on swimming speed. Integrated over the length of the fish, the red musculature from cold-acclimated fish generated 2.7, 8.9 and 5.8 times more power than the red musculature from warm-acclimated fish while swimming at 30 cm s(−)(1), 40 cm s(−)(1) and 50 cm s(−)(1), respectively. Our analysis suggests that the cold-acclimated fish should be able to swim in excess of 40 cm s(−)(1) with just their red muscle whereas the warm-acclimated fish must recruit their pink muscle well below this speed. Because the red muscle is more aerobic than the pink muscle, cold acclimation may increase the sustained swimming speed at which scup perform their long seasonal migrations at cool temperatures. We then explored the underlying mechanisms for the increase in muscle power output in cold-acclimated fish. Contrary to our expectations, cold-acclimated muscle did not have a faster relaxation rate; instead, it had an approximately 50 % faster activation rate. Our work-loop studies showed that this faster activation rate, alone, can increase the mechanical power production during cyclical contractions to a surprising extent. By driving cold-acclimated muscle through warm- and cold-acclimated in vivo conditions, we were able to partition the improvement in power production associated with increased activation rate and the approximately 20 % reduction in the duration of electromyographic activity found in the accompanying study. Depending on the position and swimming speed, approximately 60 % of the increase in power output was due to the change in the red muscle's contractile properties (i.e. faster activation); the remainder was due to the shorter stimulus duty cycle of cold-acclimated scup. Thus, by both shortening the in vivo stimulation duration and speeding up the rate of muscle activation as part of cold-acclimation, scup achieve a very large increase in the power output of their red muscle during swimming at low temperature. This increase in power output probably results in an increase in muscle efficiency and, hence, a reduction in the energetic cost of swimming. This increase in power output also reduces reliance on the less aerobic and less fatigue-resistant pink muscle. Both these abilities may increase the swimming speed at which prolonged aerobic muscle activity can occur and thus reduce the travel time for the long seasonal migrations in which scup engage.

Effects of longitudinal body position and swimming speed on mechanical power of deep red muscle from skipjack tuna (Katsuwonus pelamis)

2002 ◽  
Vol 205 (2) ◽  
pp. 189-200
Author(s):  
Douglas A. Syme ◽  
Robert E. Shadwick
Keyword(s):  
Swimming Speed ◽  
Power Output ◽  
Beat Frequency ◽  
Mechanical Power ◽  
Skipjack Tuna ◽  
Cycle Frequency ◽  
Katsuwonus Pelamis ◽  
Red Muscle ◽  
Tail Beat ◽  
Work Loop

SUMMARY The mechanical power output of deep, red muscle from skipjack tuna (Katsuwonus pelamis) was studied to investigate (i) whether this muscle generates maximum power during cruise swimming, (ii) how the differences in strain experienced by red muscle at different axial body locations affect its performance and (iii) how swimming speed affects muscle work and power output. Red muscle was isolated from approximately mid-way through the deep wedge that lies next to the backbone; anterior (0.44 fork lengths, ANT) and posterior (0.70 fork lengths, POST) samples were studied. Work and power were measured at 25°C using the work loop technique. Stimulus phases and durations and muscle strains (±5.5 % in ANT and ±8 % in POST locations) experienced during cruise swimming at different speeds were obtained from previous studies and used during work loop recordings. In addition, stimulus conditions that maximized work were determined. The stimulus durations and phases yielding maximum work decreased with increasing cycle frequency (analogous to tail-beat frequency), were the same at both axial locations and were almost identical to those used by the fish during swimming, indicating that the muscle produces near-maximal work under most conditions in swimming fish. While muscle in the posterior region undergoes larger strain and thus produces more mass-specific power than muscle in the anterior region, when the longitudinal distribution of red muscle mass is considered, the anterior muscles appear to contribute approximately 40 % more total power. Mechanical work per length cycle was maximal at a cycle frequency of 2–3 Hz, dropping to near zero at 15 Hz and by 20–50 % at 1 Hz. Mechanical power was maximal at a cycle frequency of 5 Hz, dropping to near zero at 15 Hz. These fish typically cruise with tail-beat frequencies of 2.8–5.2 Hz, frequencies at which power from cyclic contractions of deep red muscles was 75–100 % maximal. At any given frequency over this range, power using stimulation conditions recorded from swimming fish averaged 93.4±1.65 % at ANT locations and 88.6±2.08 % at POST locations (means ± s.e.m., N=3–6) of the maximum using optimized conditions. When cycle frequency was held constant (4 Hz) and strain amplitude was increased, work and power increased similarly in muscles from both sample sites; work and power increased 2.5-fold when strain was elevated from ±2 to ±5.5 %, but increased by only approximately 12 % when strain was raised further from ±5.5 to ±8 %. Taken together, these data suggest that red muscle fibres along the entire body are used in a similar fashion to produce near-maximal mechanical power for propulsion during normal cruise swimming. Modelling suggests that the tail-beat frequency at which power is maximal (5 Hz) is very close to that used at the predicted maximum aerobic swimming speed (5.8 Hz) in these fish.

scholarly journals The effect of temperature and thermal acclimation on the sustainable performance of swimming scup

2007 ◽  
Vol 362 (1487) ◽  
pp. 1995-2016 ◽  
Author(s):  
Lawrence C Rome
Keyword(s):  
Steady State ◽  
Relaxation Rate ◽  
Power Output ◽  
Muscle Power ◽  
Thermal Acclimation ◽  
The Body ◽  
Effect Of Temperature ◽  
Cold Temperatures ◽  
Duty Cycles ◽  
Red Muscle

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.

The influence of temperature on power production during swimming. I. In vivo length change and stimulation pattern

2000 ◽  
Vol 203 (2) ◽  
pp. 321-331 ◽  
Author(s):  
D.M. Swank ◽  
L.C. Rome
Keyword(s):  
Power Generation ◽  
Low Temperature ◽  
Power Output ◽  
Low Temperatures ◽  
Muscle Relaxation ◽  
Length Change ◽  
Significant Finding ◽  
Red Muscle ◽  
Effects Of Temperature

Ectothermal animals are able to locomote effectively over a wide range of temperatures despite low temperature reducing the power output of their muscles. It has been suggested that animals recruit more muscle fibres and faster fibre types to compensate for the reduced power output at low temperature, but it is not known how much low temperature actually reduces power output in vivo. ‘Optimized’ work-loop measurements, which are thought to approximate muscle function in vivo, give a Q(10) of approximately 2.3 for power output of scup (Stenotomus chrysops) red muscle between 10 degrees C and 20 degrees C. However, because of the slower muscle relaxation rate at low temperatures, ‘optimizing’ work loops requires stimulation duration to be reduced and oscillation frequency to be decreased to obtain maximal power output. Previous fish swimming experiments suggest that similar optimization may not occur in vivo, and this may have substantial consequences in terms of muscle power generation and swimming at low temperatures. To assess more precisely the effects of temperature on muscle performance and swimming, in the present study, we measured the length change, stimulation duration and stimulus phase of red muscle at various positions along scup swimming at several speeds at 10 degrees C and 20 degrees C. In a companion study, we determined the effects of temperature on in vivo power generation by driving muscle fibre bundles through these in vivo length changes and stimulation conditions, and measuring the resulting power output. The most significant finding from the present study is that, despite large differences in the in vivo parameters along the length of the fish (a decrease in stimulus duration, an increase in strain and a negative shift in phase) moving posteriorly, these parameters do not change with temperature. Thus, although the nervous system of fish could, in theory, compensate for slow muscle relaxation by greatly reducing muscle stimulation duration at low temperatures, it does not. This lack of compensation to low temperatures might reflect a potential limitation in neural control.

scholarly journals The influence of temperature on power output of scup red muscle during cyclical length changes

1992 ◽  
Vol 171 (1) ◽  
pp. 261-281 ◽  
Author(s):  
L. C. Rome ◽  
D. Swank
Keyword(s):  
Power Output ◽  
Oscillation Frequency ◽  
Maximum Power ◽  
Red Muscle ◽  
Influence Of Temperature On ◽  
Simple Extrapolation ◽  
Length Changes ◽  
Oscillation Frequencies ◽  
Work Loop

To gain insight into how temperature affects locomotory performance, we measured power output of scup red muscle during oscillatory length changes at 10 degrees C and 20 degrees C. When we optimized work loop parameters, we found that maximum power was 27.9 W kg-1 at 20 degrees C and 12.8 W kg-1 at 10 degrees C, giving a Q10 of 2.29. Maximum power was generated at a higher oscillation frequency at 20 degrees C (5 Hz) than at 10 degrees C (2.5 Hz), and the Q10 for power output at a given oscillation frequency ranged from about 1 at 1 Hz to about 5 at 7.5 Hz. An analysis of the results in terms of crossbridge kinetics suggests that the higher power output at 20 degrees C is associated with both a higher Vmax (i.e. more power per cycling crossbridge) and faster activation and relaxation (i.e. a greater number of cycling crossbridges). To obtain a more realistic understanding of the functional importance of temperature effects on muscle, we imposed on isolated muscle in vivo length changes and oscillation frequencies (measured during previous experiments on swimming scup) and the in vivo stimulus duty cycle (measured from electromyograms in this study). At 20 degrees C, muscle bundles tested under these in vivo conditions produced nearly maximal power, suggesting that the muscle works optimally during locomotion and, thus, important contractile parameters have been adjusted to produce maximum mechanical power at the oscillation frequencies and length changes needed during swimming. At 10 degrees C, muscle bundles tested under in vivo conditions produced much less power than was obtained during the ‘optimized’ work loop experiments discussed above. Furthermore, although ‘optimized’ work loop experiments showed that maximum power output occurs at 2.5 Hz, scup do not appear to swim with such a low tailbeat frequency. Although the reason for these apparent discrepancies at 10 degrees C are not known, it shows that simple extrapolation from isolated muscle to the whole animal, without knowledge of how the muscle is actually used in vivo, can be misleading.

scholarly journals Modeling red muscle power output during steady and unsteady swimming in largemouth bass

1994 ◽  
Vol 267 (2) ◽  
pp. R481-R488 ◽  
Author(s):  
T. P. Johnson ◽  
D. A. Syme ◽  
B. C. Jayne ◽  
G. V. Lauder ◽  
A. F. Bennett
Keyword(s):  
Power Output ◽  
Largemouth Bass ◽  
Muscle Power ◽  
Micropterus Salmoides ◽  
Cycle Frequency ◽  
Red Muscle ◽  
Slow Twitch ◽  
Work Done

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.

scholarly journals The influence of temperature on power production during swimming. II. Mechanics of red muscle fibres in vivo

2000 ◽  
Vol 203 (2) ◽  
pp. 333-345 ◽  
Author(s):  
L.C. Rome ◽  
D.M. Swank ◽  
D.J. Coughlin
Keyword(s):  
Power Output ◽  
Muscle Power ◽  
Muscle Performance ◽  
Muscle Fibres ◽  
Relaxation Rates ◽  
Red Muscle ◽  
The Impact ◽  
Positive Work ◽  
Muscle Power Output

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.

Power production during steady swimming in largemouth bass and rainbow trout

2000 ◽  
Vol 203 (3) ◽  
pp. 617-629 ◽  
Author(s):  
D.J. Coughlin
Keyword(s):  
Rainbow Trout ◽  
Largemouth Bass ◽  
Muscle Activity ◽  
Power Production ◽  
Emg Activity ◽  
Published Data ◽  
Red Muscle ◽  
Work Loop

Steady swimming in fishes is powered by the aerobic or red muscle, but there are conflicting theories on the relative roles of the anterior and posterior red muscle in powering steady swimming. To examine how red muscle is used to power steady swimming in rainbow trout (Oncorhynchus mykiss), electromyographic (EMG) and sonomicrometry recordings were made of muscle activity in vivo. These data were used in in vitro work-loop studies of muscle power production. Data on in vitro power production were also collected for largemouth bass (Micropterus salmoides) red muscle from previously published data on in vivo muscle activity. The in vivo data collected from swimming trout were similar to those for other species. The anterior red muscle of these fish has the longest duty cycle, the smallest phase shift between the onset of EMG activity and maximum muscle length during each tailbeat and undergoes the smallest strain or length change. For both trout and largemouth bass, work-loop experiments indicate that the majority of power for steady swimming is generated by the posterior muscle, as has been observed in other species.

The influence of thermal acclimation on power production during swimming. I. In vivo stimulation and length change pattern of scup red muscle

2001 ◽  
Vol 204 (3) ◽  
pp. 409-418 ◽  
Author(s):  
L.C. Rome ◽  
D.M. Swank
Keyword(s):  
Steady State ◽  
Power Output ◽  
Low Temperatures ◽  
Beat Frequency ◽  
Length Change ◽  
Change Pattern ◽  
Duty Cycles ◽  
Red Muscle ◽  
Tail Beat

Ectothermal animals are able to locomote in a kinematically similar manner over a wide range of temperatures. It has long been recognized that there can be a significant reduction in the power output of muscle during swimming at low temperatures because of the reduced steady-state (i.e. constant activation and shortening velocity) power-generating capabilities of muscle. However, an additional reduction in power involves the interplay between the non-steady-state contractile properties of the muscles (i.e. the rates of activation and relaxation) and the in vivo stimulation and length change pattern the muscle undergoes during locomotion. In particular, it has been found that isolated scup (Stenotomus chrysops) red muscle working under in vivo stimulus and length change conditions (measured in warm-acclimated scup swimming at low temperatures) generates very little power for swimming. Even though the relaxation of the muscle has slowed greatly, warm-acclimated fish swim with the same tail-beat frequencies and the same stimulus duty cycles at cold temperatures, thereby not affording the slow-relaxing muscle any extra time to relax. We hypothesize that considerable improvement in the power output of the red muscle at low temperatures could be achieved if cold acclimation resulted in either a faster muscle relaxation rate or in the muscle being given more time to relax (e.g. by shortening the stimulus duration or reducing the tail-beat frequency). We test these hypotheses in this paper and the accompanying paper. Scup were acclimated to 10 degrees C (cold-acclimated) and 20 degrees C (warm-acclimated) for at least 6 weeks. Electromyograms (EMGs) and high-speed cine films were taken of fish swimming steadily at 10 degrees C and 20 degrees C. At 10 degrees C, we found that, although there were no differences in tail-beat frequency, muscle strain or stimulation phase between acclimation groups, cold-acclimated scup had EMG duty cycles approximately 20 % shorter than warm-acclimated scup. In contrast at 20 degrees C, there was no difference between acclimation groups in EMG duty cycle, nor in any other muscle length change or stimulation parameter. Thus, in response to cold acclimation, there appears to be a reduction in EMG duty cycle at low swimming temperatures that is probably due to an alteration in the operation of the pattern generator. This novel acclimation probably improves muscle power output at low temperatures compared with that of warm-acclimated fish, an expectation we test in the accompanying paper using the work-loop technique.

Shortening deactivation: quantifying a critical component of cyclical muscle contraction

2021 ◽  
Author(s):  
Amy K. Loya ◽  
Sarah K. Van Houten ◽  
Bernadette M. Glasheen ◽  
Douglas M. Swank
Keyword(s):  
Power Output ◽  
Muscle Activation ◽  
Muscle Relaxation ◽  
Length Change ◽  
Isometric Tension ◽  
Energetic Cost ◽  
Muscle Shortening ◽  
Shortening Deactivation ◽  
Muscle Types ◽  
Flight Muscles

A muscle undergoing cyclical contractions requires fast and efficient muscle activation and relaxation to generate high power with relatively low energetic cost. To enhance activation and increase force levels during shortening, some muscle types have evolved stretch activation (SA), a delayed increased in force following rapid muscle lengthening. SA's complementary phenomenon is shortening deactivation (SD), a delayed decrease in force following muscle shortening. SD increases muscle relaxation, which decreases resistance to subsequent muscle lengthening. While it might be just as important to cyclical power output, SD has received less investigation than SA. To enable mechanistic investigations into SD and quantitatively compare it to SA, we developed a protocol to elicit SA and SD from Drosophila and Lethocerus indirect flight muscles (IFM) and Drosophila jump muscle. When normalized to isometric tension, Drosophila IFM exhibited a 118% SD tension decrease, Lethocerus IFM dropped by 97%, and Drosophila jump muscle decreased by 37%. The same order was found for normalized SA tension: Drosophila IFM increased by 233%, Lethocerus IFM by 76%, and Drosophila jump muscle by only 11%. SD occurred slightly earlier than SA, relative to the respective length change, for both IFMs; but SD was exceedingly earlier than SA for jump muscle. Our results suggest SA and SD evolved to enable highly efficient IFM cyclical power generation and may be caused by the same mechanism. However, jump muscle SA and SD mechanisms are likely different, and may have evolved for a role other than to increase the power output of cyclical contractions.

Dynamics of in vivo power output and efficiency of Nasonia asynchronous flight muscle

2006 ◽  
Vol 124 (1) ◽  
pp. 93-107 ◽  
Author(s):  
Fritz-Olaf Lehmann ◽  
Nicole Heymann
Keyword(s):  
Power Output ◽  
Flight Muscle
Sign in / Sign up

Export Citation Format

Share Document