Timing of head movements is consistent with energy minimization in walking ungulates

Abstract

Many ungulates show a conspicuous nodding motion of the head when walking. Until now, the functional significance of this behaviour remained unclear. Combining in vivo kinematics of quadrupedal mammals with a computer model, we show that the timing of vertical displacements of the head and neck is consistent with minimizing energy expenditure for carrying these body parts in an inverted pendulum walking gait. Varying the timing of head movements in the model resulted in increased metabolic cost estimate for carrying the head and neck of up to 63%. Oscillations of the head-neck unit result in weight force oscillations transmitted to the forelimbs. Advantageous timing increases the load in single support phases, in which redirecting the trajectory of the centre of mass (COM) is thought to be energetically inexpensive. During double support, in which-according to collision mechanics-directional changes of the impulse of the COM are expensive, the observed timing decreases the load. Because the head and neck comprise approximately 10% of body mass, the effect shown here should also affect the animals' overall energy expenditure. This mechanism, working analogously in high-tech backpacks for energy-saving load carriage, is widespread in ungulates, and provides insight into how animals economize locomotion. BackgroundThe majority of larger mammals use the quadruped walking gait as the main form of locomotion for travelling large distances [1][2][3][4][5]. Running gaits are used in bursts and for high-speed locomotion, e.g. for hunting and escaping, so an animal's life depends largely on the effective outputs of this behaviour. Nevertheless, it is the walking gait in which on average the most energy in absolute terms is consumed over an entire day [4,6,7]. As locomotion is an important energy-consuming factor for most mammals [4,[6][7][8], the main selective pressure shaping the walking gait used in slow locomotion should be energy efficiency rather than high performance.Many large mammals, such as horses, exhibit a conspicuous nodding of the head when walking. The head and neck of mammals form a highly mobile cantilever on the trunk that constitutes a substantial part of the animal's whole body mass. To date, biomechanical studies on the locomotion of quadrupedal mammals have focused almost exclusively on movements of the limbs and the trunk. The potentially energy-consuming effects of head movements relative to the trunk remain for the most part unexplored in large mammals, but have been shown to be significant in birds [9]. The few existing studies on head movements that accompany the quadrupedal mammalian walking gait [10][11][12][13][14], confirm that the head's kinematics are decoupled from the movements

The locomotor kinematics and ground reaction forces of walking giraffes

“…The phase relationship between the vertical oscillations of the neck and trunk was 15% (Fig. 8B), similar to previous findings in giraffes (Loscher et al, 2016). This suggests that mechanical energy conservation is modest with respect to supporting the weight of the head and neck.…”

“…In an adult giraffe, the mass of the head and neck accounts for approximately 10% of body mass (Mitchell et al, 2013;Simmons and Scheepers, 1996). This is similar to the proportion seen in the horse (Buchner et al, 1997), but in giraffes this mass is distributed over a longer distance, and the neck is carried with a more vertical posture (Dagg, 1962;Loscher et al, 2016).…”

“…Larger organisms such as giraffes may be particularly sensitive to this relationship, given their relatively large limb inertia. Giraffes may preferentially select stride frequencies that are optimised for metabolic economy (Loscher et al, 2016). Duty factors were consistently greater in the forelimb than in the hindlimb (Fig.…”

“…In one comparative study of ungulate neck motion (Loscher et al, 2016), the majority of walking ungulates exhibited cyclical vertical neck acceleration which was out of phase with vertical trunk acceleration. This phase relationship probably results in net kinetic energy savings and potential metabolic savings.…”

Coping with the commute: behavioural responses to wind conditions in a foraging seabird

“…Although the way in which animals move and the energetic costs accrued through movement are greatly influenced by their morphology (Aerts et al 2000, Dial 2003), many species exhibit behavioural adaptations to reduce their energy costs of transport. For example, great hammerhead sharks Sphyrna mokarran swim on their sides to exploit the greater amount of lift their abnormally large dorsal fins can then generate (Payne et al 2016), orangutans Pongo abelii sway branches to bridge gaps in the forest canopy that they otherwise must circumvent with a routeextending detour (Thorpe et al 2007 and many ungulates nod in phase with their leg movements, minimising the energy required to carry their head and neck (Loscher et al 2016). Such widespread and numerous behaviours all serve to reduce the energy cost of transport, suggesting that minimising this cost is beneficial (Halsey 2016).…”