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.

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.

Temperature effects on pH of mitochondria isolated from carp red muscle

1988 ◽  
Vol 254 (4) ◽  
pp. R611-R615 ◽  
Author(s):  
C. D. Moyes ◽  
L. T. Buck ◽  
P. W. Hochachka
Keyword(s):  
Intracellular Ph ◽  
Temperature Effects ◽  
Respiratory Control ◽  
Ph Gradient ◽  
Carp Cyprinus Carpio ◽  
Red Muscle ◽  
Effects Of Temperature ◽  
Increasing Temperature ◽  
Induced Changes

Mitochondria isolated from red muscle of carp (Cyprinus carpio) were used to investigate the effects of temperature and extramitochondrial pH (pHe) on the mitochondrial pH gradient and respiratory properties. Mitochondria from animals acclimated to 10 degrees C were isolated and incubated in KCl-based media with 0.2 mM lauroylcarnitine (C-12) as substrate. Maximal respiratory control ratios (RCR = state 3/state 4) were 16-18 between pH 6.7 and 7.4 at 10 degrees C; RCR values were 9-12 between pH 6.5 and 7.1 at 30 degrees C. Changes in RCR values were due primarily to changes in the state 3 rate (in the presence of ADP). Mitochondrial pH was determined by measuring 5,5-[2-14C]dimethyloxazolidine-2,4-dione distribution, using [14C]sucrose as an extramatrical marker. The pH gradient was inversely related to pHe. At any particular pHe, the mitochondrial pH gradient decreased with increasing temperature. However, if pHe was varied in the same manner that intracellular pH changes with temperature in vivo, the pH gradient was maintained constant at approximately 0.4 U at 10, 20, and 30 degrees C. These data suggest that carp red muscle mitochondria defend an appropriate mitochondrial pH gradient with temperature-induced changes in intracellular pH.

scholarly journals Quantifying the influence of salinity and temperature on the population dynamics of a marine ectoparasite

2016 ◽  
Vol 73 (8) ◽  
pp. 1281-1291 ◽  
Author(s):  
Maya L. Groner ◽  
Gregor F. McEwan ◽  
Erin E. Rees ◽  
George Gettinby ◽  
Crawford W. Revie
Keyword(s):  
Population Dynamics ◽  
Low Temperature ◽  
Population Growth ◽  
Low Temperatures ◽  
Sea Lice ◽  
Life Stages ◽  
Low Salinity ◽  
Linear Effects ◽  
Effects Of Temperature ◽  
Substantial Morbidity

Sea lice are common ectoparasites of farmed and wild salmonids and can cause substantial morbidity and mortality in their hosts. While sea lice infections are common in estuarine areas with variable salinity, the effects of salinity on population dynamics are poorly understood. We used existing literature to parameterize salinity-dependent logistic mortality curves for different life stages of sea lice. We then used population matrix models to characterize the effects of temperature and salinity on sea louse population growth. Our models showed that low salinity decreases survival, while low temperature retards sea louse development. In contrast with the linear effects of temperature on sea louse development, salinity has a nonlinear effect on sea louse survival; values below 20 psu cause mortality, while values above 20 psu have little effect on survival. Simulations showed that sea louse population growth can be greatest in zones that are intermediate between estuarine and oceanic. In these cases population growth is not limited by the low salinities found in more estuarine sites or the low temperatures found in more oceanic sites.

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.

scholarly journals Experimental Evolution of Enzyme Temperature Activity Profile: Selection In Vivo and Characterization of Low-Temperature-Adapted Mutants of Pyrococcus furiosus Ornithine Carbamoyltransferase

2001 ◽  
Vol 183 (3) ◽  
pp. 1101-1105 ◽  
Author(s):  
Martine Roovers ◽  
Rony Sanchez ◽  
Christianne Legrain ◽  
Nicolas Glansdorff
Keyword(s):  
Low Temperature ◽  
Kinetic Analysis ◽  
Experimental Evolution ◽  
Low Temperatures ◽  
Pyrococcus Furiosus ◽  
Ornithine Carbamoyltransferase ◽  
Yeast Mutant ◽  
Activity Profile

ABSTRACT We have obtained mutants of Pyrococcus furiosusornithine carbamoyltransferase active at low temperatures by selecting for complementation of an appropriate yeast mutant after in vivo mutagenesis. The mutants were double ones, still complementing at 15°C, a temperature already in the psychrophilic range. Their kinetic analysis is reported.

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.

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