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Preliminary title: Basis of the hummingbird flight stroke
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Authors: Hedrick, Tobalske, Ros, Warrick, Biewener
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Summary:
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Hummingbirds (Trochilidae) are widely known for their high flapping frequency and for inverting their
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wings during upstroke so as to generate lift during both halves of their flapping cycle1. We used high-
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speed stereo X-ray video recordings of hovering Ruby-Throated hummingbirds (Archilochus colubris) to
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determine the morphological and kinematic basis of this derived flight stroke. Our in vivo
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measurements reveal that inversion of the wing during upstroke occurs predominantly at the wrist and
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more distal elements while long axis rotation of the humerus is the largest single determinant of the
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overall flapping motion. Flapping by humeral rotation allows the flight muscles to produce large wing
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excursions with only small muscle contractions, facilitating high-frequency flapping. Aspects of the
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hummingbird flight stroke are exhibited by other bird species. Many other birds supinate their wings at
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the wrist during upstroke in low-speed flight2. Additionally, earlier cineradiographic3 and muscle
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activation4 studies revealed large amplitude humeral rotations of 70 to 80 degrees in the wingbeat cycle
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of the starling (Sturnis vulgaris) and pigeon (Columba livia). However, humeral rotation contributes little
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to overall wing motion in these species. Changes in the timing of rotation and the orientation of the
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humerus in hummingbirds form the basis for the shift from flapping by humeral elevation and
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depression to flapping by humeral rotation, resulting in a high gear ratio between muscle shortening
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and wing movement.
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Hummingbirds have been dubbed “vertebrate insects” due to the evolutionary convergence of wing
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kinematics, superficial body plan and even flight metabolism between these two groups5. Indeed, the
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wingbeat frequency to body mass scaling and wing loading of hummingbirds as well as their capacity for
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continuous hovering flight are more similar to those of flying insects such as fruit flies (Melanogaster
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spp.) or honeybees (Apis spp.) than they are to other birds. Early high-speed cinematography
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investigations of hummingbird flight also revealed an inverted or highly supinated wing during
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upstroke6, similar to that of many insects and allowing the bird to generate aerodynamic lift in both the
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downstroke and upstroke1. The morphological basis and evolutionary origin of wing inversion and high
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wingbeat frequency in hummingbirds have been investigated via anatomical examination of extant6 and
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fossil species7-9 along with external kinematic records provided by high speed imaging6, 10. These
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various studies produced a number of hypotheses which we tested by recording in vivo skeletal
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kinematics during hovering flight using high speed stereo X-ray videography.
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Earlier external kinematic observations revealed that the proximal feathers of the wing (the
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secondaries) do not invert completely during upstroke. This result, along with the unusually flat joint
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surfaces in the wrist and phalanges, led to the hypothesis that most of the wing inversion during
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upstroke takes place in the distal wing elements rather than at the shoulder6. This is similar in anatomic
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location to the rapid wing inversion and rotation mechanism proposed for other flying birds, some of
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which invert their wing at the wrist during upstroke of slow flight2.
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The hummingbird humerus, which is reduced in size relative to other wing bones and positioned at a
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more acute angle relative to the dorso-ventral body axis6 is also hypothesized to underlie the
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development of an insect-like flight stroke. The humeral angle has been reduced during hummingbird
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evolution as indicated by the migration of the humeral head from an orientation toward the apex of the
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bone to one perpendicular to the shaft with a pronounced proximal (?) protrusion8, 9, 11. This may enable
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extreme supination of the wing at the shoulder11, contra the external kinematic result that supination
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during upstroke is a distal wing phenomena. The acute orientation of the humerus is also hypothesized
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to facilitate high frequency flapping by allowing humeral rotation to contribute to wing flapping6.
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Our stereo X-ray videography measurements (Table 1) and µCT reconstructions (Fig. 1) revealed that
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hummingbird wing inversion during upstroke is largely due to rotation in the wrist. However, the source
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of wing rotation varies along the wing, with proximal sections influenced by proximal joints.
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Additionally, much of the wing supination could not be assigned to any of the skeletal elements,
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suggesting substantial deformation of feathers and wing soft tissue in response to inertial and
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aerodynamic forces, similar to the passive wing supination mode found in fruit flies12. The unaccounted
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for supination at the most distal site, the tip of the 4th primary, may also reflect rotation in the distal
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phalanges, which have particularly smooth and flat articulations6 (also Supp. Fig. 1) but could not be
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tracked in our recordings.
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We found that, as predicted from prior anatomical studies6, long axis rotation of the humerus plays a
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key role in the hummingbird flapping cycle (Fig. 2), providing the largest single contribution to the
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movement of the wing tip and distal leading edge (Table 2, Supp. Movies 1-4 ). Elevation and sweep at
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the shoulder also contributed to wing movement, especially at proximal and trailing-edge locations. The
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effects of flexion and rotation at the elbow and wrist were generally small.
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We compared the hummingbird humeral long axis rotation magnitude, timing, and contribution to wing
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movement with results from earlier muscle function and cineradiographic studies of starlings and
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pigeons. The magnitude of humeral rotation in the hummingbirds (Fig. 2, ~70°) was slightly less than the
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80-90° reported for pigeons and starlings with flight muscles stimulated in situ4 and the 85° estimated
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from cineradiographic records of starlings flying in a wind tunnel3. However, the contribution of
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humeral rotation to total wing tip movement was 18% in starlings, compared to 52% for the
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hummingbirds measured at a similar wing position.
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The enhanced contribution of humeral rotation to wing movement in hummingbirds is due to changes in
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the orientation of the bone and the timing of rotation. We quantified humeral orientation as the angle
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between the humerus and the leading edge of the wing. If this angle were 90°, all humeral rotation
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would contribute to flapping, while at an angle of 0° humeral rotation produces only wing supination
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and pronation. In the hummingbirds, the angle ranged from 83 ± 10° to 57 ± 6° (mean ± s.d., n=4) during
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the stroke cycle, compared to a range of 46° to 36° for the starling. Additionally, in hummingbirds,
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humeral rotational velocity was greatest near the mid-downstroke and mid-upstroke (Fig. 2); in the
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starling and pigeon rotation was most prominent at the end of upstroke and end of downstroke.
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Flapping the wing via humeral rotation facilitates a high wingbeat frequency by providing the flight
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muscles with a short moment arm but broad attachment area. A short moment arm and attendant high
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gear ratio between muscle shortening and wing movement may be necessitated by scaling relationships
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for flying birds; evidence from the Phasianidae indicates that flight muscle fascicle length increases
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isometrically13 while for birds as a whole, flapping frequencies increase with decreasing body size
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reaching 80 Hz in the smallest hummingbird species14. Thus, if the muscle strain to wing angular
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movement ratio (i.e. the muscle to wing gearing) were to remain constant, the high wingbeat
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frequencies of hummingbirds would be matched by equally high muscle strain rates, resulting in a
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reduced capacity for muscle power output15. By gearing the link between flight muscle and wing
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movement via humeral rotation, hummingbirds can use muscle strain rates16 similar to other birds,
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helping hummingbirds produce mass-specific muscle aerobic power outputs17-19 comparable or even
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greater than larger species20.
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Methods
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Three female and one male Ruby-throated hummingbirds (Archilochus colubris, 3.4 g) were captured at
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Harvard University’s Concord Field Station (CFS). During the four days of flight recording following
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capture, the birds were maintained at the CFS in individual 0.4 x 0.3 x 0.45 m cages with food and water
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provided ad libitum food and water in the form of Nektar-Plus (NEKTON®; Günter Enderle, Pforzheim,
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Baden-Württemberg, Germany) or a 20% sucrose solution (mass:volume). Prior to recording, the birds
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were marked with a set of 13 0.3-mm diameter (0.1 mg) platinum beads glued to the skin surface
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overlying the wing skeleton, vertebral column and keel of sternum to aid in X-ray reconstruction. An
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additional 6 white 0.5 mm diameter acrylic paint markers (5 µg) were added to the wings to facilitate
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tracking their movements. Following the recordings and removal of markers, two of the birds were
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released to the wild. The remaining two were sacrificed via an overdose of isoflurane inhalant for
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scanning in a µCT system (below). The experiments were performed in accordance with Harvard
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University Institutional Animal Care and Use guidelines.
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The hummingbirds were trained to fly in an 0.4 x 0.4 x 0.5 m netting enclosure and to feed from a 5 ml
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syringe filled with Nektar-Plus and positioned in the recording volume. The birds were recorded at 1000
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Hz using two X-ray videography systems composed of a Photron 1024pci camera (Photron USA Inc.)
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coupled to an X-ray C-arm system (Model 9400, OEC-Diasonics Inc., remanufactured by Radiological
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Imaging Services) and five visible-light video cameras (shutter speed 1/5000 s): one Photron SA-3, one
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Photron 1024pci, one Photron 1280pci and two Phantom v7.1 (Vision Research Inc.). The X-ray and
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light-video cameras were calibrated using direct linear transformation following pre-processing of the X-
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ray images to remove all optical distortion introduced by the multiple lenses and image intensifier21.
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Mean reprojection error across all X-ray and visible light markers was 1.3 ± 1.0 (mean ± s.d.) pixels. The
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X-ray C-arms were set to emit at 79 kVp and 10 mA.
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As noted above, µCT scans (Supp. Fig. 1) were made of the two of the hummingbirds, one posed in a
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mid-upstroke configuration and the other in mid-downstroke. Scans were performed on a (Equipment
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description) and analyzed using Mimics 13 (Materialise).
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The contributions of different joints and limb segments to total wing movement and wing supination or
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inversion were calculated by fitting a serial kinematic chain22 to the platinum markers. The chain was
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constructed, working from the proximal to distal joints, by finding the polar and long-axis rotations at
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the joint in question (Supp. Fig. 2) which brought its markers into a least-squares fit with their position in
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a canonical pose, in this case mid-downstroke. The rotations were then applied to the joint in question
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and all more distal elements. This process was then repeated at the next most proximal joint. The
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shoulder and wrist joints were permitted both polar and long axis rotations; the elbow joint was
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permitted only a polar rotation based on the observed absence of rotation between the radius and ulna
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as determined using µCT data. Contributions to total wing movement were assessed by measuring the
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path travelled by different wing points following the individual removal of rotations at different joints
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(see supplementary movies 1-4). Contributions to wing supination were assessed using the same
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approach but calculating the supination of the wing with respect to the body vertical axis and the local
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leading edge of the wing. Digitizing, X-ray reconstruction and kinematic calculations were performed
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using MATLAB 2009a (MathWorks). Following kinematic chain analysis, the 3D bone shapes were
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aligned to the X-ray video images in Maya 8.5 (Autodesk).
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Supplementary movie figure captions:
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Movie 1:
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This movie shows a lateral view of the flapping motion of a hummingbird wing with successive removal
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of the motion at different wing skeletal elements. (A.) Complete wing motion, with the path of the tip
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traced out, the wing skeletal elements tracked in our X-ray recordings in black and the rest of the wing
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surface displayed as a triangular mesh [The stroke path in part A seems inverted. I would expect it to be
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upwardly concave, like a cup]. The view is of the left wing from a point above the right wing tip. The
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bird’s anterior is to the right. All plots share the same scale and viewpoint. (B.) Flapping motion without
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the contribution of humeral sweep and elevation (but with all other contributions). (C.) Flapping motion
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without humeral long-axis rotation, but with humeral sweep and elevation. (D.) Flapping with no
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humeral motion. (E.) Flapping with no humeral or forearm (radius and ulna) movement. (F.) Flapping
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with no humeral or forearm movement or wrist sweep and elevation. (G.) Flapping with no humeral or
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forearm movement or wrist rotation. (H.) Flapping with no movement in any of the skeletal elements
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recorded in our study.
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Movie 2:
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A rear view of the wing motions from movie 1.
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Movie 3:
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An overhead view of the wing motions from movie 1.
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Movie 4:
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An above-lateral oblique view of the wing motions from movie 1.
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