The fastest and most manoeuvrable terrestrial animals are found in savannah habitats, where predators chase and capture running prey. Hunt outcome and success rate are critical to survival, so both ...predator and prey should evolve to be faster and/or more manoeuvrable. Here we compare locomotor characteristics in two pursuit predator-prey pairs, lion-zebra and cheetah-impala, in their natural savannah habitat in Botswana. We show that although cheetahs and impalas were universally more athletic than lions and zebras in terms of speed, acceleration and turning, within each predator-prey pair, the predators had 20% higher muscle fibre power than prey, 37% greater acceleration and 72% greater deceleration capacity than their prey. We simulated hunt dynamics with these data and showed that hunts at lower speeds enable prey to use their maximum manoeuvring capacity and favour prey survival, and that the predator needs to be more athletic than its prey to sustain a viable success rate.
A. V. Hill was awarded the 1922 Nobel Prize, jointly with Otto Meyerhof, for Physiology or Medicine for his work on energetic aspects of muscle contraction. Hill used his considerable mathematical ...and experimental skills to investigate the relationships among muscle mechanics, biochemistry and heat production. The main ideas of the work for which the Nobel Prize was awarded were superseded within a decade, and the legacy of Hill and Meyerhof's Nobel work was not a set of persistent, influential ideas but rather a prolonged period of extraordinary activity that advanced the understanding of how muscles work far beyond the concepts that led to the Nobel Prize. Hill pioneered the integration of mathematics into the study of physiology and pharmacology. Particular aspects of Hill's own work that remain in common use in muscle physiology include mathematical descriptions of the relationships between muscle force output and shortening velocity and between force output and calcium concentration, and the model of muscle as a contractile element in series with an elastic element. We describe some of the characteristics of Hill's broader scientific activities and then outline how Hill's work on muscle energetics was extended after 1922, as a result of Hill's own work and that of others, to the present day.
figure legend A. V. Hill's scientific legacy. A. V. Hill (pictured) and his colleague Otto Meyerhof shared the 1922 Nobel Prize for Physiology or Medicine. Seven enduring elements of Hill's legacy to muscle physiology are shown. Arrows link concepts and approaches to related disciplines where they have been foundational and highly influential.
Videos of free swimming of catsharks (
Scyliorhinus canicula
) were analysed to give values of swimming speed (units: FL (fish lengths) s
−1
), stride-length (forward movement in the direction of ...travel per cycle of body undulation (units: FL) and stride-frequency (units: s
−1
). Most of the swims (139 of 163, 85%) were at speeds less than 0.545 FL s
−1
and were categorized as slow. The rest (24/163, 15%) were categorized as fast. Stride-lengths and stride-frequencies could be evaluated for 115 of the slow swims and 16 of the fast swims. We discuss the fast swim results, but there were so few fast swims that no firm conclusions could be made. As swim speed increased during slow swims, there was a strong increase stride-length slope 0.965, P < 0.0001) and a small increase in stride-frequency. Most stride-frequencies (70/115, 61%) were in the range 0.68–0.88 s
−1
. Previous experiments on red muscle isolated of catshark showed that in this range of frequencies of sinusoidal movement, high power was produced at high efficiency (Curtin and Woledge
b
). Lower frequencies gave less power and at higher frequencies the efficiency of energy conversion was lower. Thus, we conclude that during routine swimming catsharks choose a swimming speed that optimizes red muscle performance in terms of power and efficiency.
Large mammals that live in arid and/or desert environments can cope with seasonal and local variations in rainfall, food and climate
by moving long distances, often without reliable water or food en ...route. The capacity of an animal for this long-distance travel is substantially dependent on the rate of energy utilization and thus heat production during locomotion-the cost of transport
. The terrestrial cost of transport is much higher than for flying (7.5 times) and swimming (20 times)
. Terrestrial migrants are usually large
with anatomical specializations for economical locomotion
, because the cost of transport reduces with increasing size and limb length
. Here we used GPS-tracking collars
with movement and environmental sensors to show that blue wildebeest (Connochaetes taurinus, 220 kg) that live in a hot arid environment in Northern Botswana walked up to 80 km over five days without drinking. They predominantly travelled during the day and locomotion appeared to be unaffected by temperature and humidity, although some behavioural thermoregulation was apparent. We measured power and efficiency of work production (mechanical work and heat production) during cyclic contractions of intact muscle biopsies from the forelimb flexor carpi ulnaris of wildebeest and domestic cows (Bos taurus, 760 kg), a comparable but relatively sedentary ruminant. The energetic costs of isometric contraction (activation and force generation) in wildebeest and cows were similar to published values for smaller mammals. Wildebeest muscle was substantially more efficient (62.6%) than the same muscle from much larger cows (41.8%) and comparable measurements that were obtained from smaller mammals (mouse (34%)
and rabbit (27%)). We used the direct energetic measurements on intact muscle fibres to model the contribution of high working efficiency of wildebeest muscle to minimizing thermoregulatory challenges during their long migrations under hot arid conditions.
Skinned fibres have advantages for comparing the muscle properties of different animal species because they can be prepared from a needle biopsy taken under field conditions. However, it is not clear ...how well the contractile properties of skinned fibres reflect the properties of the muscle fibres in vivo. Here, we compare the mechanical performance of intact fibre bundles and skinned fibres from muscle of the same animals. This is the first such direct comparison. Maximum power and isometric force were measured at 25 °C using peroneus longus (PL) and extensor digiti-V (ED-V) muscles from wild rabbits (Oryctolagus cuniculus). More than 90% of the fibres in these muscles are fast-twitch, type 2 fibres. Maximum power was measured in force-clamp experiments. We show that maximum power per volume was the same in intact (121.3 ± 16.1 W l(-1), mean ± s.e.m.; N=16) and skinned (122.6 ± 4.6 W l(-1); N=141) fibres. Maximum relative power (power/F(IM) Lo, where F(IM) is maximum isometric force and Lo is standard fibre length) was also similar in intact (0.645 ± 0.037; N=16) and skinned (0.589 ± 0.019; N=141) fibres. Relative power is independent of volume and thus not subject to errors in measurement of volume. Finally, maximum isometric force per cross-sectional area was also found to be the same for intact and skinned fibres (181.9 kPa ± 19.1; N=16; 207.8 kPa ± 4.8; N=141, respectively). These results contrast with previous measurements of performance at lower temperatures where skinned fibres produce much less power than intact fibres from both mammals and non-mammalian species.
Muscle fiber contraction involves the cyclical interaction of myosin cross-bridges with actin filaments, linked to hydrolysis of ATP that provides the required energy. We show here the relationship ...between cross-bridge states, force generation, and Pi release during ramp stretches of active mammalian skeletal muscle fibers at 20°C. The results show that force and Pi release respond quickly to the application of stretch: force rises rapidly, whereas the rate of Pi release decreases abruptly and remains low for the duration of the stretch. These measurements show that biochemical change on the millisecond timescale accompanies the mechanical and structural responses in active muscle fibers. A cross-bridge model is used to simulate the effect of stretch on the distribution of actomyosin cross-bridges, force, and Pi release, with explicit inclusion of ATP, ADP, and Pi in the biochemical states and length-dependence of transitions. In the simulation, stretch causes rapid detachment and reattachment of cross-bridges without release of Pi or ATP hydrolysis.
Muscle dysfunction is a common feature of severe sepsis and multiorgan failure. Recent evidence implicates bioenergetic dysfunction and oxidative damage as important underlying pathophysiological ...mechanisms. Increased abundance of uncoupling protein-3 (UCP3) in sepsis suggests increased mitochondrial proton leak, which may reduce mitochondrial coupling efficiency but limit reactive oxygen species (ROS) production. Using a murine model, we examined metabolic, cardiovascular, and skeletal muscle contractile changes following induction of peritoneal sepsis in wild-type and Ucp3(-/-) mice. Mitochondrial membrane potential (Δψm) was measured using two-photon microscopy in living diaphragm, and contractile function was measured in diaphragm muscle strips. The kinetic relationship between membrane potential and oxygen consumption was determined using a modular kinetic approach in isolated mitochondria. Sepsis was associated with significant whole body metabolic suppression, hypothermia, and cardiovascular dysfunction. Maximal force generation was reduced and fatigue accelerated in ex vivo diaphragm muscle strips from septic mice. Δψm was lower in the isolated diaphragm from septic mice despite normal substrate oxidation kinetics and proton leak in skeletal muscle mitochondria. Even though wild-type mice exhibited an absolute 26 ± 6% higher UCP3 protein abundance at 24 h, no differences were seen in whole animal or diaphragm physiology, nor in survival rates, between wild-type and Ucp3(-/-) mice. In conclusion, this murine sepsis model shows a hypometabolic phenotype with evidence of significant cardiovascular and muscle dysfunction. This was associated with lower Δψm and alterations in mitochondrial ATP turnover and the phosphorylation pathway. However, UCP3 does not play an important functional role, despite its upregulation.
Muscle samples were taken from the gluteus, semitendinosus and longissimus muscles of a captive cheetah immediately after euthanasia. Fibres were 'skinned' to remove all membranes, leaving the ...contractile filament array intact and functional. Segments of skinned fibres from these cheetah muscles and from rabbit psoas muscle were activated at 20°C by a temperature-jump protocol. Step and ramp length changes were imposed after active stress had developed. The stiffness of the non-contractile ends of the fibres (series elastic component) was measured at two different stress values in each fibre; stiffness was strongly dependent on stress. Using these stiffness values, the speed of shortening of the contractile component was evaluated, and hence the power it was producing. Fibres were analysed for myosin heavy chain content using gel electrophoresis, and identified as either slow (type I) or fast (type II). The power output of cheetah type II fibre segments was 92.5±4.3 W kg(-1) (mean ± s.e., 14 fibres) during shortening at relative stress 0.15 (the stress during shortening/isometric stress). For rabbit psoas fibre segments (presumably type IIX) the corresponding value was significantly higher (P<0.001), 119.7±6.2 W kg(-1) (mean ± s.e., 7 fibres). These values are our best estimates of the maximum power output under the conditions used here. Thus, the contractile filament power from cheetah was less than that of rabbit when maximally activated at 20°C, and does not account for the superior locomotor performance of the cheetah.
Background: Phosphate is released by the cardiac actomyosin ATPase during contraction.
Results: Stretching active cardiac muscle decreases phosphate release within milliseconds.
Conclusion: ...Mechanical stimuli such as stretch cause an immediate change in actomyosin ATPase kinetics.
Significance: Stretch facilitates a powerful contraction by increasing cross-bridges in a pre-power stroke state, and changes cytoplasmic phosphate flux, which may influence energetic homeostasis.
The contractile performance of the heart is linked to the energy that is available to it. Yet, the heart needs to respond quickly to changing demands. During diastole, the heart fills with blood and the heart chambers expand. Upon activation, contraction of cardiac muscle expels blood into the circulation. Early in systole, parts of the left ventricle are being stretched by incoming blood, before contraction causes shrinking of the ventricle. We explore here the effect of stretch of contracting permeabilized cardiac trabeculae of the rat on the rate of inorganic phosphate (Pi) release resulting from ATP hydrolysis, using a fluorescent sensor for Pi with millisecond time resolution. Stretch immediately reduces the rate of Pi release, an effect observed both at full calcium activation (32 μmol/liter of Ca2+), and at a physiological activation level of 1 μmol/liter of Ca2+. The results suggest that stretch redistributes the actomyosin cross-bridges toward their Pi-containing state. The redistribution means that a greater fraction of cross-bridges will be poised to rapidly produce a force-generating transition and movement, compared with cross-bridges that have not been subjected to stretch. At the same time stretch modifies the Pi balance in the cytoplasm, which may act as a cytoplasmic signal for energy turnover.
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