Rules to fly by: pigeons navigating horizontal obstacles limit steering by selecting gaps most aligned to their flight direction

Abstract

Flying animals must successfully contend with obstacles in their natural environments. Inspired by the robust manoeuvring abilities of flying animals, unmanned aerial systems are being developed and tested to improve flight control through cluttered environments. We previously examined steering strategies that pigeons adopt to fly through an array of vertical obstacles (VOs). Modelling VO flight guidance revealed that pigeons steer towards larger visual gaps when making fast steering decisions. In the present experiments, we recorded three-dimensional flight kinematics of pigeons as they flew through randomized arrays of horizontal obstacles (HOs). We found that pigeons still decelerated upon approach but flew faster through a denser array of HOs compared with the VO array previously tested. Pigeons exhibited limited steering and chose gaps between obstacles most aligned to their immediate flight direction, in contrast to VO navigation that favoured widest gap steering. In addition, pigeons navigated past the HOs with more variable and decreased wing stroke span and adjusted their wing stroke plane to reduce contact with the obstacles. Variability in wing extension, stroke plane and wing stroke path was greater during HO flight. Pigeons also exhibited pronounced head movements when negotiating HOs, which potentially serve a visual function. These head-bobbing-like movements were most pronounced in the horizontal (flight direction) and vertical directions, consistent with engaging motion vision mechanisms for obstacle detection. These results show that pigeons exhibit a keen kinesthetic sense of their body and wings in relation to obstacles. Together with aerodynamic flapping flight mechanics that favours vertical manoeuvring, pigeons are able to navigate HOs using simple rules, with remarkable success.

Pigeons (C. livia) Follow Their Head during Turning Flight: Head Stabilization Underlies the Visual Control of Flight

“…These translational head movement patterns during low-speed turns are similar to the head bobbing observed in pigeons prior to landing and reminiscent of the head bobbing observed during walking in many bird species, both of which are thought to provide visual cues for landing and object localization (Davies and Green, 1988 ; Green, 1998 ). Recently, we found similar head speed fluctuations associated with vertical and horizontal obstacle negotiation flight in pigeons (Ros et al, 2017 ) Consequently, peaks in translational head speed during turning flight (Figure 3 ) may also serve to improve parallax-based perception of speed and depth by increasing translational optic flow (Dunlap and Mowrer, 1930 ; Nakayama, 1985 ; Koenderink, 1986 ; Davies and Green, 1988 ; Zeil et al, 2008 ; Eckmeier et al, 2013 ). In addition, troughs in head speed (Figure 3 ) may function to reduce motion blur, facilitate detection of independently moving objects and, possibly, dishabituate ganglion cells involved in motion sensing (Frost and DiFranco, 1976 ; Nakayama, 1985 ; Necker, 2007 ; Frost, 2009 ).…”

“…Importantly, the pigeon's head stabilization strategy isolates its head from body motions (Figures 3C , 4A,B ; see Videler et al, 1983 ; Bilo et al, 1985 ; Warrick et al, 2002 ; Eckmeier et al, 2008 ; Kress et al, 2015 ; Ros et al, 2017 ). As a result, both translational and angular head and body movements are uncorrelated, demonstrating reduced mechanical coupling effects between the head and body (Figures 3C , 4A,B ).…”

“…However, it is unclear whether the delay between head side-slip immediately following a head saccade and the corresponding aerodynamic roll/pitch body rotations that occur in the next downstroke may be controlled through a dedicated visuomotor pathway. Recordings of in vivo muscle activation referenced to wing stroke timing (Ros et al, 2017 ) show that the onset of pectoralis muscle activation powering the downstroke occurs 23 ± 9 ms after the end of a saccade, when head side-slip is maximal. Temporal delays involved in optic flow processing via the AOS in birds at present, however, are unknown (Frost et al, 1990 ; Arends and Zeigler, 1991 ; Eckmeier et al, 2013 ).…”

Obstacle traversal and route choice in flying honeybees: Evidence for individual handedness

“…The challenge of finding a suitable route through a cluttered environment is faced not just by honeybees, but by a number of animal species, including birds, that inhabit dense vegetation [ 14 , 20 ]. Toads, for example, are able to gauge the width of a gap between two obstacles from afar, and decide whether to go through the gap or circumvent it, depending upon its width [ 21 ].…”

Coevolving advances in animal flight and aerial robotics

“…Inspired by this finding, they suggest that knowing which kind of wing damage may affect aerial robot performance most could inspire more robust robot designs. Finally, Ros et al [13] contrast the challenge of flying through vertically oriented versus horizontally oriented clutter, by studying how pigeons fly through artificial forests. They found that, in comparison with flight past vertical obstacles, pigeons manoeuvred past horizontal obstacles faster and with less effort by selecting gaps most in line with their flight direction.…”