Minimizing the cost of locomotion with inclined trunk predicts crouched leg kinematics of small birds at realistic levels of elastic recoil

Abstract

Small birds move with pronograde trunk orientation and crouched legs. Although the pronograde trunk has been suggested to be beneficial for grounded running, the cause(s) of the specific leg kinematics are unknown. Here we show that three charadriiform bird species (northern lapwing, oystercatcher, and avocet; great examples of closely related species that differ remarkably in their hind limb design) move their leg segments during stance in a way that minimizes the cost of locomotion. We imposed measured trunk motions and ground reaction forces on a kinematic model of the birds. The model was used to search for leg configurations that minimize leg work that accounts for two factors: elastic recoil in the intertarsal joint, and cheaper negative muscle work relative to positive muscle work. A physiological level of elasticity (∼0.6) yielded segment motions that match the experimental data best, with a root mean square of angular deviations of ∼2.1 deg. This finding suggests that the exploitation of elastic recoil shapes the crouched leg kinematics of small birds under the constraint of pronograde trunk motion. Considering that an upright trunk and more extended legs likely decrease the cost of locomotion, our results imply that the cost of locomotion is a secondary movement criterion for small birds. Scaling arguments suggest that our approach may be utilized to provide new insights into the motion of extinct species such as dinosaurs.

The influence of speed and size on avian terrestrial locomotor biomechanics: Predicting locomotion in extinct theropod dinosaurs

“…Previous studies have indicated that terrestrial locomotion in modern birds is considerably different from that in humans. Birds employ a crouched, digitigrade, parasagittal posture, whereby the femur is subhorizontally oriented for much of the stride, and where the majority of limb movement occurs at the knee, driven by the ‘hamstring’ muscles [ 19 – 33 ]. This reflects the location of their whole-body centre of mass (COM), which is markedly anterior to the hips [ 31 , 34 ].…”

“…As a reaction force, it represents the summation of accelerations of all the individual components of the body during movement, and is fundamental to understanding the forces, moments and stresses occurring within the limbs of an animal during locomotion [ 7 , 35 , 51 – 56 ]. Despite its importance, the GRF has been measured in relatively few species of birds, in the course of investigating other biomechanical parameters [ 26 , 30 , 33 , 35 , 37 , 40 , 46 , 53 , 57 – 61 ]. Hence, not enough is currently known about how the GRF varies in time and space throughout the stance phase in different bird species, or how this varies with speed or body size, to the point that quantitative predictions may be made for other theropods (avian or non-avian).…”

Postural control during quiet bipedal standing in rats

“…Studies using monkeys have reported differences in bipedal and quadrupedal walking (Japanese macaque [ 7 – 10 ], bonobo [ 11 ], reviewed in [ 12 ]) and the evolution of human walking (chimpanzee [ 13 ], reviewed in [ 14 ]). Studies using birds have discussed the energetic effect required for the transition from walking to running (guinea fowl [ 15 ], emu and ostrich [ 16 ], lapwing, oystercatcher, and avocet [ 17 ]). Moreover, animal models of neural ataxia, such as monkey models of Parkinson’s disease (transgenic [ 18 , 19 ], neurotoxin [ 20 ], reviewed in [ 21 , 22 ]), stroke (reviewed in [ 23 ]), and spinal cord injury have been investigated.…”

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

“…Further, alternative hypotheses relating to the implications of elbow/knee orientation concerning directional stability [43] or passive release of elastic energy facilitating protraction [44] should not be dismissed, especially for highly cursorial quadrupeds. And multi-segment limbs may well offer multiple advantages, from facilitating elastic storage and recoil (see [13]) with implications in terms of passive joint stabilization (Seyfarth et al, 2001 [45]). However, the benefit proposed here of reduction in joint work given a generally low limb-work force profile appears potentially very general, and applicable to parasagittal quadrupeds of diverse scales, evolutionary backgrounds (consider chameleon), and even orientations (remember sloth).…”

“…This was attributed to an absence-or at least insufficiency-of multi-joint linkages to provide inter-joint power transfer [11], meaning that minimization of joint work was taken as a suitable initial cost function to consider when exploring animal limb design (though see also [12]). Minimization of joint work does appear effective in accounting for some features of bipedal [13] and quadrupedal [14,15] gait kinetics [1]. But force vectors in bipeds (humans: [16]; birds: [17]; wallabies: [18]) and quadrupeds [19] are consistently observed to be orientated between axial and vertical.…”