Richard L. Marsh

Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs

SUMMARY The function of many muscles during natural movements is to accelerate a mass. We used a simple model containing the essential elements of this functional system to investigate which musculoskeletal features are important for increasing the mechanical work done in a muscle-powered acceleration. The muscle model consisted of a muscle-like actuator with frog hindlimb muscle properties, operating across a lever to accelerate a load. We tested this model in configurations with and without a series elastic element and with and without a variable mechanical advantage. When total muscle shortening was held constant at 30%, the model produced the most work when the muscle operated with a series elastic element and an effective mechanical advantage that increased throughout the contraction (31 J kg-1 muscle vs 26.6 J kg-1 muscle for the non-compliant, constant mechanical advantage configuration). We also compared the model output with the dynamics of jumping bullfrogs, measured by high-speed video analysis, and the length changes of the plantaris muscle, measured by sonomicrometry. This comparison revealed that the length, force and power trajectory of the body of jumping frogs could be accurately replicated by a model of a fully active muscle operating against an inertial load, but only if the model muscle included a series elastic element. Sonomicrometer measurements of the plantaris muscle revealed an unusual, biphasic pattern of shortening, with high muscle velocities early and late in the contraction, separated by a period of slow contraction. The model muscle produced this pattern of shortening only when an elastic element was included. These results demonstrate that an elastic element can increase the work output in a muscle-powered acceleration. Elastic elements uncouple muscle fiber shortening velocity from body movement to allow the muscle fibers to operate at slower shortening velocities and higher force outputs. A variable muscle mechanical advantage improves the effectiveness of elastic energy storage and recovery by providing an inertial catch mechanism. These results can explain the high power outputs observed in jumping frogs. More generally, our model suggests how the function of non-muscular elements of the musculoskeletal system enhances performance in muscle-powered accelerations.

Adaptations of the Gray Catbird Dumetella carolinensis to Long-Distance Migration: Flight Muscle Hypertrophy Associated with Elevated Body Mass

The size and composition (lean-dry, water, and fat contents) of the flight muscles of the catbird were investigated as a function of the large seasonal changes in body mass which occur in this species. The mass of the pectoralis muscle is highly positively correlated with body mass, leading to an elevation in muscle mass of ∼35% during fall premigratory fattening. The changes in muscle mass are brought about by coordinated variations in all major components of the muscles which were measured. High-oxidative, fast-twitch fibers represent 88% of the total fibers in the pectoralis muscle. The cross-sectional area of the muscle fibers increases proportional to muscle mass, suggesting that fiber hypertrophy may underlie the changes in muscle mass. Calculations of the power available from the muscles compared with the aerodynamic power required by catbirds in flight indicates that augmentation of pectoralis muscle mass could make a significant contribution to flight performance.

Effects of exercise on the biomechanical, biochemical and structural properties of tendons.

Tendon has been shown to undergo remodeling in response to strength or endurance training, however, compared to muscle, studies of the effects of exercise on tendon are limited and the information is inconsistent. Exercise may influence the structure, chemical composition and/or mechanical properties of tendon. Studies that have examined mechanical changes of tendon in response to endurance training suggest that ultimate failure strength and stiffness increase with training. Available reports indicate that increases in tensile strength and stiffness are probably not associated with increases in collagen concentration or with tendon hypertrophy. The paucity of data renders it impossible to evaluate the response of other structural, chemical and mechanical parameters to training. Furthermore, few investigators have included discrete measures of structural, biomechanical and biochemical variables within a single study. The lack of integrative studies makes it difficult to definitively associate changes in the mechanical properties of tendon with chemical composition and structure.

Seasonal and Geographic Variation of Cold Resistance in House Finches Carpodacus mexicanus

The house finch (Carpodacus mexicanus) is resident in tropical and subtropical regions as well as in localities having relatively severe winters. The extent of its winter acclimatization was assessed in freshly captured individuals of this species from southern California and Colorado. In severe cold stress tests involving exposure to Ta < −60 C, the former did not remain homeothermic any longer in winter than in late spring, whereas the Colorado birds did (8.8 vs. 97.5 min; P < .001). The capacity for winter acclimatization evident in these Colorado individuals was correlated with modest winter fattening, a response lacking in those from southern California. Freshly captured house finches from coastal Massachusetts were also studied in winter. These birds, whose ancestors were introduced to the Atlantic seaboard from California in 1940, remained homeothermic at Ta < −60 C for a period that was significantly longer and shorter than the ones for winter house finches from southern California and Colorado, respectively. The labile character of cold resistance in house finches was further established by study of birds captured in southern California and maintained in an outdoor aviary in Ann Arbor, Michigan. After 6 mo in captivity these birds showed a level of cold resistance in January-February similar to that observed in free-living Colorado birds in winter. Evidence is assembled suggesting that winter acclimatization is primarily metabolic in captive as well as free-living house finches.

The energetic costs of trunk and distal-limb loading during walking and running in guinea fowl Numida meleagris: I. Organismal metabolism and biomechanics.

SUMMARY We examined the energetic cost of loading the trunk or distal portion of the leg in walking and running guinea fowl (Numida meleagris). These different loading regimes were designed to separately influence the energy use by muscles used during the stance and swing phases of the stride. Metabolic rate, estimated from oxygen consumption, was measured while birds locomoted on a motorized treadmill at speeds from 0.5 to 2.0 m s-1, either unloaded, or with a mass equivalent to 23% of their body mass carried on their backs, or with masses equal to approximately 2.5% of their body mass attached to each tarsometatarsal segment. In separate experiments, we also measured the duration of stance and swing in unloaded, trunk-loaded, or limb-loaded birds. In the unloaded and limb-loaded birds, we also calculated the mechanical energy of the tarsometatarsal segment throughout the stride. Trunk and limb loads caused similar increases in metabolic rate. During trunk loading, the net metabolic rate (gross metabolic rate - resting metabolic rate) increased by 17% above the unloaded value across all speeds. This percentage increase is less than has been found in most studies of humans and other mammals. The economical load carriage of guinea fowl is consistent with predictions based on the relative cost of the stance and swing phases of the stride in this species. However, the available comparative data and considerations of the factors that determine the cost of carrying extra mass lead us to the conclusion that the cost of load carrying is unlikely to be a reliable indicator of the distribution of energy use in stance and swing. Both loading regimes caused small changes in the swing and/or stance durations, but these changes were less than 10%. Loading the tarsometatarsal segment increased its segmental energy by 4.1 times and the segmental mechanical power averaged over the stride by 3.8 times. The increases in metabolism associated with limb loading appear to be linked to the increases in mechanical power. The delta efficiency (change in mechanical power divided by the change in metabolic power) of producing this power increased from 11% in walking to approximately 25% in running. Although tarsometatarsal loading was designed to increase the mechanical energy during swing phase, 40% of the increase in segmental energy occurred during late stance. Thus, the increased energy demand of distal limb loading in guinea fowl is predicted to cause increases in energy use by both stance- and swing-phase muscles.

Winter fattening in the american goldfinch and the possible role of temperature in its regulation

We investigated whether environmental temperature has any causal role in the winter fattening in certain finches of the subfamily Carduelinae. Correlational analyses between fat content of American goldfinches (Carduelis tristis) and various short- and long-term measures of temperature provide no evidence for a proximate role of this environmental variable in determining the degree of fattening of these birds in southeastern Michigan. Their fat content shows the best correlations (r = −.61 to −.63) with the long-term average minimum temperature or record low temperature for the date of capture. Furthermore, inclusion of long-term thermal measures in multivariate analyses excludes from significance temperature conditions surrounding the day of capture. Comparison of American goldfinches wintering in Michigan, California, and Texas, respectively, strengthens the conclusion that environmental temperature does not directly influence their fat content. Taken together, our data on this species favor the hypothesis that temperature is an ultimate, i.e., evolutionarily significant, rather than a proximate factor in winter fattening. Comparisons of American goldfinches, pine siskins (Carduelis pinus), and common redpolls (Carduelis flammea) in Michigan indicate that these similar-sized congeners show different levels of winter fattening under similar winter conditions. The differences in fat content among these species do not correlate in any simple way with their respective overall winter distributions.

Blood flow in guinea fowl Numida meleagris as an indicator of energy expenditure by individual muscles during walking and running

Running and walking are mechanically complex activities. Leg muscles must exert forces to support weight and provide stability, do work to accelerate the limbs and body centre of mass, and absorb work to act as brakes. Current understanding of energy use during legged locomotion has been limited by the lack of measurements of energy use by individual muscles. Our study is based on the correlation between blood flow and aerobic energy expenditure in active skeletal muscle during locomotion. This correlation is strongly supported by the available evidence concerning control of blood flow to active muscle, and the relationship between blood flow and the rate of muscle oxygen consumption. We used injectable microspheres to measure the blood flow to the hind‐limb muscles, and other body tissues, in guinea fowl (Numida meleagris) at rest, and across a range of walking and running speeds. Combined with data concerning the various mechanical functions of the leg muscles, this approach has enabled the first direct estimates of the energetic costs of some of these functions. Cardiac output increased from 350 ml min−1 at rest, to 1700 ml min−1 at a running speed (∼2.6 m s−1) eliciting a of 90% of . The increase in cardiac output was achieved via approximately equal factorial increases in heart rate and stroke volume. Approximately 90% of the increased cardiac output was directed to the active muscles of the hind limbs, without redistribution of blood flow from the viscera. Values of mass‐specific blood flow to the ventricles, ∼15 ml min−1 g−1, and one of the hind‐limb muscles, ∼9 ml min−1 g−1, were the highest yet recorded for blood flow to active muscle. The patterns of increasing blood flow with increasing speed varied greatly among different muscles. The increases in flow correlated with the likely fibre type distribution of the muscles. Muscles expected to have many high‐oxidative fibres preferentially increased flow at low exercise intensities. We estimated substantial energetic costs associated with swinging the limbs, co‐contraction to stabilize the knee and work production by the hind‐limb muscles. Our data provide a basis for evaluating hypotheses relating the mechanics and energetics of legged locomotion.

Performance of guinea fowl Numida meleagris during jumping requires storage and release of elastic energy

SUMMARY The ability of birds to perform effective jumps may play an important role in predator avoidance and flight initiation. Jumping can provide the vertical acceleration necessary for a rapid takeoff, which may be particularly important for ground-dwelling birds such as phasianids. We hypothesized that by making use of elastic energy storage and release, the leg muscles could provide the large power outputs needed for achieving high velocities after takeoff. We investigated the performance of the leg muscles of the guinea fowl Numida meleagris during jumping using kinematic and force-plate analyses. Comparison of the methods indicated that in this species the wings did not supply energy to power takeoff and thus all the work and power came from the leg muscles. Guinea fowl produced a peak vertical force of 5.3 times body weight. Despite having lower muscle-mass-specific power output in comparison to more specialized jumpers, guinea fowl demonstrated surprisingly good performance by producing muscle-mass-specific work outputs of 45 J kg–1, a value approximately two thirds of the maximal expected value for skeletal muscle. The muscle-mass-specific peak power output during jumping was nearly 800 W kg–1, which is more than twice the peak isotonic power estimated for guinea fowl leg muscles. To account for high power outputs, we concluded that energy has to be stored early in the jumps and released later during peak power production, presumably using mechanisms similar to those found in more specialized jumpers.

Measurement of Maximum Oxygen Consumption in Guinea Fowl Numida meleagris Indicates That Birds and Mammals Display a Similar Diversity of Aerobic Scopes during Running

Judgement of exercise performance in birds has been hampered by a paucity of data on maximal aerobic capacity. We measured the maximal rate of oxygen consumption (V̇o2, max) in running guinea fowl Numida meleagris, a bird that has been used in several previous studies of avian running. Mean V̇o2, max during level treadmill running was 97.5 ± 3.7 mL O2 kg−1 min−1 (mean ± SEM, N = 5). V̇o2, max was on average 6% higher when the birds ran uphill compared with the value during level running (paired t‐test, P = 0.041, N = 5). The mean basal rate of oxygen consumption (V̇o2, bmr) of the same individuals was 7.9 ± 0.5 mL O2 kg−1 min−1. Mean factorial aerobic scope based on individually measured values of V̇o2, max and V̇o2, bmr was 13.2 ± 0.6 (mean ± SEM, N = 5). This value was considerably lower than the factorial aerobic scope previously measured during running in Rhea americana, a large flightless ratite. The difference in factorial scope between these two running birds likely reflects the effects of body size as well as size‐independent differences in the ability to deliver and use oxygen. These data confirm a previous prediction that birds have a diversity of factorial aerobic scopes similar to that exhibited by mammals.

The energetic costs of trunk and distal-limb loading during walking and running in guinea fowl Numida meleagris: II. Muscle energy use as indicated by blood flow.

SUMMARY We examined the changes in muscle energy use in guinea fowl running at 1.5 m s-1 either unloaded, or carrying trunk loads equal to 23% of body mass, or loads on their distal legs equal to a total of 5% of body mass. We estimated muscle energy use by measuring blood flow to all of the leg muscles using injected microspheres. Total blood flow to the leg muscles increased by approximately 15% under both loading conditions, which matched the percentage increase in net organismal metabolic rate. Significant increases in energy use (inferred from blood flow) above that found in unloaded birds were found in 12 muscles in trunk-loaded birds, with most of the increases restricted to stance-phase muscles, as predicted. Just three of these muscles, the femerotibialis, the iliotibialis lateralis pars postacetabularis and the fibularis longus accounted for 70% of the increased energy use. Noticeably absent from the group of muscles that increased energy use during trunk loading were several large biarticular muscles that have extensor actions at the hip or ankle, but flexor actions at the knee. We concluded that the low energetic cost of carrying trunk loads in guinea fowl may rely on the activation of a group of muscles that together provide support and propulsion across all the major joints, without producing opposing moments at other joints that could potentially waste energy. The specific leg muscles responsible for the increase in metabolism during trunk loading also suggest that the energy cost of producing mechanical work may be an important determinant of the cost of carrying extra mass on the trunk. During distal-limb loading, eleven leg muscles had significant increases in energy use, but unlike during trunk loading, both stance- and swing-phase muscles had large increases in energy use. This distribution of energy use between stance and swing agrees with the prediction that increased mechanical work determines the cost of limb loading, because a substantial fraction of the increased segmental work during distal-limb loading in guinea fowl has been found to occur during stance.