Ontogenetic scaling of pelvic limb muscles, tendons and locomotor economy in the Ostrich (Struthio camelus)

Abstract

In rapidly growing animals there are numerous selective pressures and developmental constraints underpinning the ontogenetic development of muscle-tendon morphology and mechanical properties. Muscle force generating capacity, tendon stiffness, elastic energy storage capacity and efficiency were calculated from muscle and tendon morphological parameters and in vitro tendon mechanical properties obtained from a growth series of ostrich cadavers. Ontogenetic scaling relationships were established using reduced major axis regression analysis. Ostrich pelvic limb muscle mass and cross-sectional area broadly scaled with positive allometry, indicating maintained or relatively greater capacity for maximum isometric force generation in larger animals. The length of distal limb tendons was found to scale with positive allometry in several tendons associated with antigravity support and elastic energy storage during locomotion. Distal limb tendon stiffness scaled with negative allometry with respect to body mass, with tendons being relatively more compliant in larger birds. Tendon material properties also appeared to be size-dependent, suggesting that the relative increased compliance of tendons in larger ostriches is due in part to compensatory distortions in tendon material properties during maturation and development, not simply from ontogenetic changes in tendon geometry. Our results suggest that the previously reported increase in locomotor economy through ontogeny in the ostrich is due to greater potential for elastic energy storage with increasing body size. In fact, the rate of this increase may be somewhat greater than the conservative predictions of previous studies, thus illustrating the biological importance of elastic tendon structures in adult ostriches.

Ontogenetic changes of hindlimb muscle mass in Cabot's tragopan (Galliformes, Phasianidae) and their functional implications

“…In the greater rhea, the total limb muscle mass scaled with an exponent of 1.18 when tendons were included in the measurements; for individual muscles, M. tibialis cranialis and M. puboischiofemoralis showed isometric growth, and the remaining 17 muscles scaled with positive allometry (Picasso, 2015). Using a series of 18 samples aged from hatchling to 2 years, Channon et al (2019) considered 21 muscles in the ostrich and found that either total muscle mass, or individual muscle mass, scaled with strong positive allometry. However, in the emu, another precocial ratite bird, a comprehensive study showed that the muscle masses presented three scaling patterns: 26 muscles out of 34 were positively allometric, FPPD2 was negatively allometric, and 7 muscles (AM, FCL, FME, ITM, ITCR, ISF, IFI) were isometric (Lamas et al, 2014).…”

“…Compared with the hip and thigh muscle group, the shank muscles are characterized by having obvious long tendons. Through ontogeny, these tendons undergo positive allometric or persistent isometric growth, suggesting that they may have enhanced or at least equivalent potential for elastic energy storage with increasing body size (Bennett, 1996;Channon et al, 2019;Lamas et al, 2014). Considering the muscle-tendon unit as a whole, a trade-off between muscle force and tendon elasticity should exist to provide economy and efficiency of locomotion during ontogeny.…”

“…Intraspecific scaling studies are less common, and the trends for scaling of muscle morphology in growing animals are less clear. The most comprehensive data are from the studies of the ratites, and suggest that positive allometry predominates in the growth of muscle mass (Lamas et al, 2014;Picasso, 2015;Channon, Young, Cordner, & Swann, 2019). This suggests not only that muscle forces are likely to be maintained to support body mass during growth within a species, but also that adult limbs may be specifically adapted for enhanced muscle power production which favors to attain relatively high running speeds (Lamas et al, 2014;Picasso, 2015).…”

From fibre to function: are we accurately representing muscle architecture and performance?

“…Ontogenetic changes in muscle architecture have also been studied in a range of other species [e.g. emu Dromaius novaehollandiae (Lamas et al ., 2014); ostrich (Channon et al ., 2019); eastern cottontail rabbit Sylvilagus floridanus (Butcher et al ., 2019); rat Rattus norvegicus domestica (Woittiez et al ., 1986)], including analyses of the contribution of differences in muscle properties to disparate gait, energetics and maximal performance in male versus female chickens across sexual maturity (Rose et al ., 2016a,b).…”