On vision in birds: coordination of head-bobbing and gait stabilises vertical head position in quail

Abstract

IntroductionHead-bobbing in birds is a conspicuous behaviour related to vision comprising a hold phase and a thrust phase. The timing of these phases has been shown in many birds, including quail, to be coordinated with footfall during locomotion. We were interested in the biomechanics behind this phenomenon. During terrestrial locomotion in birds, the trunk is subjected to gait-specific vertical oscillations. Without compensation, these vertical oscillations conflict with the demands of vision (i.e., a vertically stable head position). We tested the hypothesis that the coordination between head-bobbing and trunk movement is a means of reconciling the conflicting demands of vision and locomotion which should thus vary according to gait.ResultsSignificant differences in the timing of head-bobbing were found between gaits. The thrust phase was initiated just prior to the double support phase in walking (vaulting) trials, whereas in running (bouncing) trials, thrust started around midstance. Altering the timing of head-trunk-coordination in simulations showed that the timing naturally favoured by birds minimizes the vertical displacement of the head. When using a bouncing gait the timing of head bobbing had a compensatory effect on the fluctuation of the potential energy of the bird’s centre of mass.ConclusionThe results are consistent with expectations based on the vertical trunk fluctuations observed in biomechanical models of vaulting and bouncing locomotion. The timing of the head-bobbing behaviour naturally favoured by quail benefits vision during vaulting and bouncing gaits and potentially helps reducing the mechanical cost associated with head bobbing when using a bouncing gait.

Mixed gaits in small avian terrestrial locomotion

“…At first view, mixed gaits seem to confer disadvantages in terms of visual cue (cf. discussion in 10 20 ) and leg load, because of the larger CoM vertical amplitudes and GRF imbalance. In addition, our simulations indicate that mixed gaits are less efficient than grounded running at same system energies.…”

“…One explanation for these findings may lie in the pronograde trunk position in birds. Together, trunk, neck, and head make more than 80% of the total mass of an individual, and have a relative motion with respect to the leg (the trunk oscillates about the hip) so that leg compression and releases do not necessary oscillate in phase with trunk rotation 10 20 28 29 . Such a phase shift may vary based on the relation between the inertia of the trunk, the torque in the hip joint, and viscoelastic properties in the leg.…”

“…However, our model predicts mixed gaits for only 5% of the solutions when using walking-like parameters and only 2% when using bouncing-like parameters, while the measured birds employ it in a large percentage of their strides. We think there are some possibilities to explain this paradox: a) birds might use very frequently a combination of leg parameters that are close to the attraction zone of mixed gaits, b) locomoting without visual flow might represent a disturbance to the animal enforcing such mixed gait patterns due to the relation between trunk motions and head bobbing 20 29 , or c) our simple 2D model, which has identical leg parameters and lacks of medio-lateral motions, fails in showing the complete solution space for mixed gaits. To investigate possibility ‘b,’ experiments with projected environments moving matched to the treadmill’s speed would be helpful.…”

“…If this is the case, as speed increases, one can expect that %congruity values will cross a value of 50, which is usually defined as a boundary between walking-like and running-like gaits (e.g. 7 19 20 ). In this ‘transition zone’, small fluctuations, as birds experience on a treadmill or face in irregular natural environments, might produce %congruity shifts to either walking or running mechanics.…”

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

“…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…”