Variation in limb loading magnitude and timing in tetrapods

Abstract

Comparative analyses of locomotion in tetrapods reveal two patterns of stride cycle variability. Tachymetabolic tetrapods (birds and mammals) have lower inter-cycle variation in stride duration than bradymetabolic tetrapods (amphibians, lizards, turtles and crocodilians). This pattern has been linked to the fact that birds and mammals share enlarged cerebella, relatively enlarged and heavily myelinated Ia afferents, and γ-motoneurons to their muscle spindles. Both tachymetabolic tetrapod lineages also possess an encapsulated Golgi tendon morphology, thought to provide more spatially precise information on muscle tension. The functional consequence of this derived Golgi tendon morphology has never been tested. We hypothesized that one advantage of precise information on muscle tension would be lower and more predictable limb bone stresses, achieved in tachymetabolic tetrapods by having less variable substrate reaction forces than bradymetabolic tetrapods. To test this hypothesis, we analyzed hindlimb substrate reaction forces during locomotion of 55 tetrapod species in a phylogenetic comparative framework. Variation in species means of limb loading magnitude and timing confirm that, for most of the variables analyzed, variance in hindlimb loading and timing is significantly lower in species with encapsulated versus unencapsulated Golgi tendon organs. These findings suggest that maintaining predictable limb loading provides a selective advantage for birds and mammals by allowing energy savings during locomotion, lower limb bone safety factors and quicker recovery from perturbations. The importance of variation in other biomechanical variables in explaining these patterns, such as posture, effective mechanical advantage and center-of-mass mechanics, remains to be clarified.

Testing the propulsive role of m. peroneus longus during quadrupedal walking in Varanus exanthematicus

“…These data from phylogenetically and anatomically disparate lizard species speak to the conserved nature of motor patterns during locomotion (Cuff et al, 2019; Goslow, Dial & Jenkins, 1989; Lauder & Shaffer, 1988; Peters & Goslow, 1983; Wainwright, Sanford, Reilly, & Lauder, 1989). Considering the sprawling posture and limb kinematics shared between many squamates (Granatosky et al, 2019b), it is possible that m. peroneus longus may have a minor role in propulsion even in species without an enlarged lateral calcaneal heel (Reilly, 1995), although the propulsive moment arm of the muscle would be smaller. Thus, the propulsive role of m. peroneus longus in V. exanthematicus was probably built upon existing muscle activity patterns present in ancestral squamates and then exaggerated through modifications to lateral calcaneal heel and the associated proximal expansion of the fifth metatarsal (Sullivan, 2010).…”

“…Only strides in which the animal was traveling in a straight path and not accelerating or decelerating (i.e., steady‐state locomotion) were selected for analysis. Steady‐state locomotion was determined by calculating the instantaneous velocity of a digitized point on the head between subsequent video frames throughout the entire stride, and then using regression analysis to determine whether velocity changed during the stride (Granatosky & Schmitt, 2019; Granatosky et al, 2019b). Only strides in which no change in speed (i.e., slope not significantly different than zero) was detected were analyzed.…”

Limb work and joint work minimization reveal an energetic benefit to the elbows-back, knees-forward limb design in parasagittal quadrupeds

“…It should be noted that some more basal lepidosaurs do not follow the general quadrupedal pattern, but further taxonomic sampling is required to assess whether there is any biological consistency to this finding. Data for the timing of peak vertical force in the hindlimb was reported by Granatosky et al [38]. Data for the timing of peak vertical force in the forelimb previously unpublished (see electronic supplementary material, table S1).…”

Bear Locomotion

“…Such a finding indicates that pacing may constitute a similar invariant repetitive behavior similar to patients with autism. However, Granatosky et al (2020) note that locomotor rhythmicity is a normal component of bird and mammal locomotion independent of pacing behaviors. The factors that predispose bears to pacing in zoos may be linked to large home range size, large daily travel distance, or large body size (Mason and Clubb 2004).…”