© 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb186270. doi:10.1242/jeb.186270 RESEARCH ARTICLE Gliding for a free lunch: biomechanics of foraging flight in common swifts (Apus apus) Tyson L. Hedrick1,*,Cécile Pichot2 and Emmanuel de Margerie2,* ABSTRACT temporal (5–100 Hz) resolution, even for species where use of an Although the biomechanics of animal flight have been well studied in on-board satellite-based positioning package is currently infeasible laboratory apparatus such as wind tunnels for many years, the because of weight or other restrictions. Application of video applicability of these data to natural flight behaviour has been measurement methods has already revealed flight speeds well examined in few instances and mostly in the context of long-distance beyond those achieved in wind tunnels by quantifying mating or migration. Here, we used rotational stereo-videography to record the display behaviour in common swifts (Henningsson et al., 2010) and free-flight trajectories of foraging common swifts. We found that, hummingbirds (Clark, 2009), along with high-speed turns and despite their exquisite manoeuvring capabilities, the swifts only rarely pursuits in cliff swallows (Shelton et al., 2014). Field trajectory performed high-acceleration turns. More surprisingly, we also found recordings also revealed energy extraction from the ground to air that despite feeding on tiny insects probably moving with ambient wind speed gradient by foraging barn swallows (Warrick et al., flow, the birds adjust their air speed to optimize cost of transport over 2016). In the recordings of the present study, the common swifts distance. Finally, swifts spent only 25% of their time flapping; the were also engaged in foraging, permitting comparison with the majority of their time (71%) was spent in extended wing gliding, during foraging flight dynamics of two evolutionarily distinct coursing which the average power expended for changes in speed or elevation aerial insectivores (swallows and swifts) as well as comparison of was 0.84 W kg−1 and not significantly different from 0. Thus, gliding natural and wind tunnel flight in swifts. swifts extracted sufficient environmental energy to pay the cost of The prior wind tunnel studies on gliding (Henningsson and flight during foraging. Hedenström, 2011) and flapping flight (Henningsson et al., 2011a, b) in swifts and models of the effect of wind speed and direction on KEY WORDS: Glide polar, Kinematics, Rotational stereo optimal bird airspeed (Pennycuick, 1978) provide a series of videography, Soaring, Thermal, Wind testable hypotheses on how flight biomechanics relate to flight behaviour. First, the observed flight performance in gliding and INTRODUCTION flapping is expected to conform to the glide polar and flight power Common swifts (Apus apus) are coursing aerial insectivores known curves measured in wind tunnel experiments, with swifts losing to spend the majority of their life on the wing, even sleeping while in potential energy during gliding and adding kinetic or potential flight and staying in the air for up to 10 months at a time energy while flapping. Wind tunnel experiments with live birds (Hedenström et al., 2016). However, breeding and rearing their (Henningsson and Hedenström, 2011) and preserved wings young tie the birds to a particular location and require local foraging (Lentink et al., 2007) measured maximum lift to drag ratios in along with frequent returns to the nest. This provides an opportunity gliding flight of 12.5 and 10.0, respectively, at flight speeds of 9.5 for quantifying free-flight foraging biomechanics with high spatial and 9.0 m s−1. This is also close to the preferred flight speed of a and temporal resolution for comparison with data collected from swift in flapping flight in a wind tunnel (Henningsson et al., 2011b) wind tunnel experiments (e.g. Henningsson and Hedenström, 2011; and thus the modal airspeed of free-flying swifts is hypothesized to Henningsson et al., 2011a; Lentink et al., 2007) and linking these be near 9 m s−1. Extreme flight speeds reached by swifts during underlying biomechanical performance measures to natural flight group social bonding-related events (Henningsson et al., 2010) are behaviour. not expected to appear in foraging flight behaviour as these are Here, we quantified swift flight trajectories by rotational stereo likely to be costly and of little use in capturing small, slow-moving videography (RSV), which uses a camera and telephoto lens with a prey. Second, theory predicts (Pennycuick, 1978), and studies of set of mirrors to combine views from two vantage points into one migrating or commuting birds have confirmed (e.g. Hedenström image, all mounted on an instrumented pivot to track individual et al., 2002; Kogure et al., 2016; Wakeling and Hodgson, 1992), that birds during flight (de Margerie et al., 2015). Application of this and birds should adjust their airspeed when flying upwind or downwind other videographic methods enables measurement of field flight for energetically optimal cost of transport over ground. However, biomechanics with high spatial (centimetre–metre scale) and swifts forage mostly on small aerial prey: mainly aphids, complemented with ant, fly, beetle or spider species of less than 1University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. 2CNRS, 5 mm length, depending on location and season (Lack and Owen, Universitéde Rennes, Normandie Univ., EthoS (Ethologie animale et humaine)- 1955; Gory, 2008). Because these species belong to aeroplankton UMR 6552, F-35000 Rennes, France. and move with the wind (Geerts and Miao, 2005; Wainwright et al., *Authors for correspondence ([email protected]; 2017), we hypothesize that swifts optimize transport in the air [email protected]) (rather than ground) reference frame and thus do not adjust airspeed with wind speed. Third, foraging barn swallows appear to extract T.L.H., 0000-0002-6573-9602; C.P., 0000-0003-0510-1946; E.d.M., 0000-0002- 5380-3355 energy from vertical wind shear accessible in their near-ground foraging activities. Common swifts typically forage higher in the Received 7 June 2018; Accepted 10 September 2018 atmosphere where vertical wind shear should be less common but Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2018) 221, jeb186270. doi:10.1242/jeb.186270 (30–50 s) were added to the dataset, along with categorical List of symbols and abbreviations information on flight behaviour for all recordings (flapping, a acceleration vector in the air reference frame, adjusted to gliding, etc.), based on detailed observation of RSV images at account for ρ 30 Hz, downsampled to match the 6 Hz position recording A wind speed vector frequency. RSV recordings contained an average of 2.9% (14.4 F magnitude of centripetal acceleration frames, 2.4 s) of missing positions, caused by difficulties in keeping g magnitude of gravitational acceleration m body mass the bird within the RSV field of view. These missing positions were P mass-specific rate of change in kinetic and potential energy interpolated during smoothing because the smoothing operations Pk mass-specific rate of change in kinetic energy require continuous data, but were later removed from the Pp mass-specific rate of change in potential energy biomechanical analysis. R radius of curvature RSV rotational stereo videography Smoothing S wing area s ground speed This kinematics-focused examination of the swift foraging dataset v velocity vector in the ground reference frame used a different smoothing method from the previous foraging va velocity vector in the air reference frame, adjusted to ecology analysis (de Margerie et al., 2018), with more attention account for ρ given to correctly smoothing the velocities and accelerations. The U airspeed, adjusted to account for ρ RSV method natively produces position measurements in a X ground reference Cartesian position in the X direction, spherical coordinate system Θ, Φ, Ρ (i.e. azimuthal angle, computed from smoothed inputs Ρ Y ground reference Cartesian position in the Y direction, elevation angle and radius), with a measurement uncertainty for Ρ2 computed from smoothed inputs that increases proportional to and is a fixed property of the device Z ground reference Cartesian position in the Z direction, for Θ and Φ (de Margerie et al., 2015). The cumulative outcome of computed from smoothed inputs these uncertainties in 3D Cartesian space is a random position Θ azimuthal angle measurement from RSV uncertainty attaining 0.2, 0.8 and 1.8 m at 100, 200 and 300 m, ρ air density respectively. Because Ρ varies widely within each recording, we ρ 0 air density at standard temperature and pressure Θ Φ Ρ used a smoothing spline with per-point error tolerance for , and radial distance measurement from RSV Ρ Φ elevation angle measurement from RSV determined by these theoretical considerations to smooth the raw · dot-over character, indicating first derivative with respect to coordinate data. Once the smoothed spherical coordinate quantities time Θs, Φs, Ρs were determined, they were converted to Cartesian ·· double dot-over character, indicating second derivative with coordinates X,Y,Z for further analysis without application of any respect to time additional smoothing. Smoothed first and second derivatives of Subscript e equivalent airspeed or a quantity based on equivalent airspeed position with respect to time (i.e. X_ ; Y_ ; Z_ and X€; Y€; Z€) were Subscript s smoothed computed by differentiating the smoothing spline functions for _ € _ _ _ Θ, Φ and Ρ to produce Qs; Qs, etc. We computed X ; Y; Z and X€; Y€; Z€ from these values, using the derivatives of the underlying we hypothesize that they take advantage of other environmental spherical to Cartesian conversion equations, e.g.: energy sources such as thermals to reduce the cost of foraging. ¼ ðF Þ; ð Þ Lastly, barn swallow flight manoeuvres during foraging are Z Ps sin s 1 typically low energy and the birds appear to depend on a fast Z_ ¼ sinðF ÞP_ þ cosðF ÞP F_ ; ð2Þ approach to unsuspecting prey rather than a sharp turn to catch s s s s s evasive prey (Warrick et al., 2016).