Mechanical function of two ankle extensors in wild turkeys: shifts from energy production to energy absorption during inclineversusdecline running

Abstract

SUMMARYWe investigated the mechanical function of two ankle extensor muscles, the lateral gastrocnemius (LG) and peroneus longus (PL), in wild turkeys Meleagris gallopavo during steady speed running. We hypothesized that mechanical work output of the LG and PL during running parallels the demand for mechanical work on the body. The turkeys ran on level, inclined (+6°,+12°) and declined (–6°, –12°) treadmills to change the demand for mechanical work. Simultaneous measurements of muscle length(from sonomicrometry) and muscle force (from tendon strain gauges) were used to calculate mechanical work output.During level running at a speed of 2 m s–1, the LG and PL were both active in stance but produced peak force at different times, at approximately 21% of stance duration for the LG and 70% for the PL. The LG and PL also had different length patterns in stance during level running. The LG underwent little shortening during force production, resulting in negligible net positive work (2.0±0.8 J kg–1). By contrast, the PL produced force across a stretch–shorten cycle in stance and did significant net positive work (4.7±1.6 J kg–1). Work outputs for both the LG and PL were directly proportional to running slope. When we increased the demand for net positive work by running the turkeys on an incline, the LG and PL increased stance net positive work output in direct proportion to slope (P<0.05). Stance net positive work output increased to 7.0±1.3 J kg–1 for the LG and 8.1±2.9 J kg–1 for the PL on the steepest incline. Increases in stance net positive work for the LG and PL were associated with increases in net shortening strain and average shortening velocity, but average force in stance remained constant. The LG and PL muscles were also effective energy absorbers during decline running, when there is demand for net negative work on the body. During decline running at 2 m s–1 on the steepest slope, the LG absorbed 4.6±2.2 J kg–1 of net work in stance and the PL absorbed 2.4±0.9 J kg–1 of net work. Shifts in muscle mechanical function from energy production during incline running to energy absorption during decline running were observed over a range of running speeds from 1–3 m s–1 for both the LG and PL.Two fundamentally different mechanisms for changing work output were apparent in the mechanical behavior of the LG and PL. The LG simply altered its length pattern; it actively shortened during incline running to produce mechanical energy and actively lengthened during decline running to absorb mechanical energy. The PL changed mechanical function by altering its length pattern and by shifting the timing of force production across its stretch–shorten cycle. During incline running, the PL produced force during late stance shortening for positive work, but during decline running,the timing of force production shifted into early stance, to align with lengthening for negative work. In addition, during decline running, the PL greatly reduced or eliminated late stance shortening, thus reducing the potential for positive work.Our results show that the changing demands for whole body work during steady speed running are met, at least in part, by an ability of single muscles to shift mechanical function from net energy production to net energy absorption.

Leg muscles that mediate stability: mechanics and control of two distal extensor muscles during obstacle negotiation in the guinea fowl

“…Furthermore, horse distal tendons are prone to injury and heat damage [38,39]. In contrast, the ankle extensors of generalists such as ducks, guinea fowl and turkeys, store relatively less elastic energy, but probably have higher safety factors and can control work against the environment for other tasks, such as swimming (ducks) and incline running (guinea fowl, turkeys) [11][12][13]40]. This and other recent studies suggest that distal extensor muscles also play a critical role in stability by rapidly adjusting work output in response to terrain perturbations [18,19,21].…”

“…In vivo studies suggest that the DF contributes more than LG to elastic energy cycling in steady running, but does not contribute to work for incline running [12]. By contrast, the LG contributes moderately to elastic energy cycling, and also contributes to work on an incline [11][12][13].…”

“…Both these muscles have pinnate, short-fibred architecture with a relatively long free tendon. The LG and DF function similarly during steady level locomotion to provide economic weight support during stance and facilitate tendon elastic energy cycling [11][12][13].…”

Muscle power attenuation by tendon during energy dissipation

“…(a) Surgery and muscle-tendon unit instrumentation Instrumentation procedures were identical to earlier studies [4,11], and therefore only briefly described here. Birds were induced and maintained on 2 to 4 per cent inhalable isoflurane anaesthesia throughout sterile surgical procedures.…”

“…Such 'drop-landings' are probably among the highest-powered decelerations in locomotion [21,22]. We used wild turkeys for this study, as their distal leg muscles have calcified tendons that allow for accurate measurements of muscle force [4,11]. Independent calculations of whole MTU length (from video-based joint kinematics and tendon travel experiments) and direct measurements of muscle fascicle length (from sonomicrometry) allowed us to determine the length trajectory, and thus the function, of the series elastic tendon.…”