Mechanics of wing-assisted incline running (WAIR)
Flight Laboratory, Division of Biological Sciences, The University of Montana, Missoula, MT, 59812, USA
* Author for correspondence (e-mail: mbundle{at}selway.umt.edu)
Accepted 14 August 2003
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Summary |
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Key words: accelerometry, force platform, inclined running, climbing flight, origin of flight, wing-assisted incline running (WAIR), chukar partridge, Alectoris chukar
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Introduction |
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WAIR has been documented in the juveniles and adults of four species of
ground birds, and involves the simultaneous use of flapping wings and running
legs to ascend steep inclines (Dial,
2003). WAIR permits extant ground birds, and may have permitted
proto-birds, to use their hindlimbs more effectively in retreat to elevated
refuges (cliffs, boulders, trees, etc.). It has been hypothesized that as
these animals negotiate precipitous inclines (>60°), they alter their
normal flight stroke to develop aerodynamic forces that secure the animal's
feet upon the substrate, essentially functioning like the spoiler on a
racecar, to enhance traction (Dial,
2003
).
From previous work (Dial,
2003) we knew that chukars Alectoris chukar engaged in
WAIR were able to run up vertical obstacles. We also knew that hatchlings as
young as 3 days old use their partial wings to assist ascents, and that
week-old hatchlings could ascend inclines unmatched by manipulated individuals
whose flight feathers had been removed. Yet on a smooth inclined substrate
there were no measurable performance differences between experimental groups,
suggesting that the winged animals were not simply flying up the incline.
Further, the reported preliminary measures of instantaneous acceleration from
birds engaged in WAIR (Dial,
2003
) suggest that during the late stages of the wing's
downstroke, the birds' center of mass (COM) experiences an acceleration that
is directed towards the substrate. Despite the relevance of these observations
to discussions on the evolution of bird flight and the likely importance of
WAIR to the natural history of ground birds in general, much remains unknown
about this form of locomotion.
In this paper, we address the mechanics of WAIR through two primary
questions. First, do the wings of chukars perform distinct functions during
WAIR and free flight? The only published data of whole-body acceleration
during WAIR (Dial, 2003) do
not permit this critical comparison. Second, if differences in wing function
exist between WAIR and free flight, do the wings enable the hindlimbs to
generate large ground reaction forces (GRFs) when animals negotiate
precipitous inclines? In other words, do the hindlimbs of these animals
generate useful forces during ascents, or do they instead perform a
non-propulsive role (e.g. balance)?
To evaluate the hypothesis that during WAIR ground birds use their wings to adhere themselves to the substrate to improve hindlimb function, we measured the instantaneous acceleration of the COM during WAIR and during free flight at a similar climb angle. Since acceleration is the only vector component of the total force, the direction of the acceleration of the COM is the same as the direction of total force. We predicted that during a substantial portion of the wingbeat cycle the acceleration of the birds' COM would be directed towards the substrate during WAIR, but not during flight.
To determine the extent to which hindlimbs are active during bouts of WAIR, we mounted a force platform in a ramp that could be inclined to angles between horizontal (0°) and vertical (90°) (Fig. 1). Thus, we would be able to measure the GRF generated during foot strikes as the birds engaged in WAIR over steep incline angles, including vertical. We specifically hypothesized that hindlimb force generation would provide a substantial portion of the required external work at all inclines, including 90° (Fig. 1).
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Materials and methods |
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Birds were trained to ascend an inclined treadmill, the speed of which was selected to slow but not eliminate the animal's rate of climb. The birds were also trained to run up a ramp housing a force platform that could be inclined at angles between horizontal and vertical. Finally, the chukars were trained to take off on command from a marker and to fly at an angle to a platform.
Data acquisition
Accelerometers
To investigate whole-body instantaneous accelerations during WAIR and free
flights, we employed two separate protocols. During both protocols the
recording from, and harnessing of, the accelerometers were identical. The WAIR
protocol required birds harnessed with the accelerometers to ascend a
treadmill inclined to 52°. This permitted accelerometer recordings from a
series of consecutive wing beats, but did not ensure that birds achieved or
maintained a steady velocity. The treadmill was used specifically to lengthen
the duration of the bout of WAIR, not to achieve a steady state condition.
The free-flight protocol required birds harnessed with the accelerometers to fly with a climb angle similar to that imposed during the treadmill-induced WAIR. Birds were trained to fly on command to an elevated perch 2.3 m high. They were placed at a horizontal distance of 1.6 m from the base of the perch so that their average climb angle was similar to the angle of inclination of the treadmill (i.e. 52°).
Two uni-axial accelerometers (EGAX-10, Entran, Fairfield, NJ, USA) with a sensitivity range of ±10 times the acceleration due to gravity (g) were aligned orthogonally and fused with self-catalyzing cyanoacrylate. The two accelerometers (mass 0.5 g each without leads) were mounted in foam and secured with athletic tape to form a package that could be mounted on the back of the animals. The dimensions of this `backpack' were 3 cm x 1.5 cm with a height of 1.5 cm. Two bound strands of four-lead shielded lightweight cable (Cooner Wire, Chatsworth, CA, USA) exited the backpack and connected the accelerometers to an amplifier and power supply (Vishay 2100 system strain gauge conditioner and amplifier, Measurements Group, Inc., Raleigh, NC, USA). The analog signals from the strain gauge amplifier were acquired to a computer through a 16-bit A/D board (Digidata 1322A, Axon Instruments, Inc., Union City, CA, USA) at 3333.3 Hz, using Axoscope 8.1 software. Short tabs of tape extended from the long axes of the backpack and were securely sutured to the bird's intervertebral ligaments. The most posterior portion of the backpack lay immediately anterior to the synsacrum; this location was 3 cm dorsal and 3 cm posterior to the COM of the carcass of an adult chukar. Our choice of attachment site was based on this location's close proximity to the COM and the strong inter-vertebral ligaments to which the backpack could be attached without influencing the animal's performance. This site also ensured the alignment of the accelerometers with the standard anatomical body axes, such that one accelerometer lay in the anterior-posterior (A-P) plane while the second accelerometer lay in the dorso-ventral (D-V) plane. We assume that the location described above experiences accelerations that are representative of those of the true center of mass throughout the course of the wingbeat cycle.
The accelerometers were calibrated at the end of each recording session by alternately placing them in orientations where they were parallel and then orthogonal to the acceleration due to gravity. This process was repeated at least six times and the mean voltage difference between the two orientations was determined to be the voltage output produced by an acceleration of 9.8 m s-2.
Force platform
A force plate (25 cm x 10 cm), previously described by Biewener
(1983), was used to measure
GRFs over different inclines during WAIR. The force plate was mounted flush in
a moveable ramp, and overlaid with 50-grit sandpaper to reduce slippage. The
force plate uses strain gauges in a Wheatstone bridge circuit to give separate
voltage outputs proportional to the normal (two channels, fore and aft) and to
the parallel (a single channel) components of the force acting on it. The
strain gauges were powered by a Vishay 2100 system strain gauge conditioner
and amplifier (Measurements Group, Inc., Raleigh, NC, USA). Analog signals
from the amplifier were converted to digital through the same 16-bit A/D board
we described above.
The force-plate channels sensitive to the normal component of force were calibrated by placing ten different masses (range 0.040-2.245 kg) at 2 cm increments along the length of the plate to establish a relationship between foot-strike position and the fore or aft channel most sensitive to pressure at that location. The channel sensitive to parallel force was calibrated by tilting the force plate by 90° and then suspending seven masses (range 0.05-2.00 kg) attached to the center of the plate by an inelastic cord. During testing with static weights at angles where a weight would remain stationary on the force plate (between 30° and 45°). we were able to predict the mass of known weights to within 2.2±0.5%, mean ± standard deviation (S.D.).
During recording sessions the angle of inclination of the force plate was increased in 10° increments between 60° and 90°. Only trials with a single foot strike where the entire foot was on the force plate were included in the analysis (a representative trial is reproduced in Fig. 2). Throughout these experiments we make the assumption that the wake produced by the animal's wings during WAIR does not influence the recordings of the force plate. We justify this assumption with the knowledge that the width of the force plate was only slightly larger than the width of the animal's body 10 cm vs 9 cm, and that the chukar's wing length of 24 cm issufficiently long, relative to the width of the plate, that vortices shed by these structures are likely to occur lateral to the forceplate.
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High-speed video recordings
Simultaneous high-speed video recordings (Redlake Masd Inc., PCI 500,
250-500 frames s-1, shutter speed 1/2500-1/5000) were obtained
during all experiments, using two internally synchronized cameras placed
lateral to the path of motion. One of the cameras supplied detailed images of
the force-plate strike during runs, or lift-off during flights. The second
camera provided a wide-angle image to allow whole-body velocity measurements
over the entire run. For each run, the video recordings were terminated by an
external trigger that permitted synchronization of video recordings with the
accelerometer and force-plate data.
Data analysis
Frames of reference
Both the accelerometers and the force plate have axes of direct measurement
that are dependent on the orientation of the instruments during the
experimental protocol (Fig. 1).
For both the force plate and the accelerometers the component axes were summed
to yield a resultant vector in the frame of reference of the instrument. To
compare resultant vectors obtained during different experimental conditions
(e.g. across inclines), the calculated vectors were rotated from the frame of
reference of the instrument to the global frame of reference. Vectors with an
orientation of 0° or 360° were parallel to the unit vector (0,1). The
degree of rotation was determined from the orientation of the measuring device
at the moment of interest.
Accelerometer data
The accelerometer data were zeroed to eliminate DC offset and filtered with
an interpolative smoothing spline in Igor Pro version 4.0 (Wavemetrics, Inc.,
OR, USA) before further analysis, which was performed in Microsoft Excel 2000
(Microsoft Corp., Redmond, WA, USA). The orientation of the accelerometers
throughout the trial was determined from the video recording by digitizing a
line parallel to the bird's back (Video point 2.1, Lenox Softworks, Lenox, MA,
USA and Microsoft Excel 2000). The calibrated recordings from the A-P and D-V
component accelerometers (Fig.
2) were combined to obtain a resultant acceleration vector. The
orientation of this vector was adjusted to the global frame of reference, by a
rotation that depended on the angle of inclination of the bird's back. The
unit vector (0,1) was added to the resultant vector so that by convention, the
accelerometers would read 1 g oriented at 360° for a
motionless bird resting on the floor.
The mismatch in sampling frequency between the accelerometer data and the high-speed video, typically 3333.3 and 500 Hz, respectively, was overcome by averaging the resultant acceleration vectors collected in the time interval between two video frames and assigning the average vector a time value that would correspond to the first frame. Following this calculation we obtained measurements of the magnitude and direction of the acceleration of the COM that correspond directly to each image recorded by the high-speed video cameras.
Kinematic data were obtained from the video recordings corresponding to the analyzed portion of each trial. We noted the instant of each start of downstroke (SDS) and each end of downstroke (EDS) kinematic event that occurred within the analyzed portion. We determined the downstroke and upstroke transitions based on the movements of the bird's wrist. From these data the video frames falling midway and two-thirds of the way between SDS and EDS were determined and labeled mid-downstroke (MDS) and two-thirds downstroke (0.66DS). The frames falling one-third and mid-way between the kinematic events EDS and the following SDS were identified as one-third upstroke (0.33US) and mid-upstroke (MUS).
Force-plate data
The inclination of the force platform during each trial was determined from
the video recordings by digitizing a line parallel to the force platform. The
force-platform data were also zeroed to eliminate DC offset and filtered with
an interpolative smoothing spline in Igor Pro version 4.0 (Wavemetrics, Inc.)
before further analysis, which was performed in Microsoft Excel 2000. The
normal force component was calculated through a position-dependent, weighted
average between the calibrated fore and aft channels using the digitized
location of the foot on the plate. The parallel force component was converted
from volts (V) to Newtons (N) using the calibration algorithm previously
described for the parallel force channel. The normal and parallel components
of the GRF (Fig. 2) were summed
to yield the GRF. The orientation of this vector was rotated by the angle of
the incline to obtain vectors in the global frame of reference. The GRF
vectors calculated for the time interval between successive video frames were
averaged and assigned to the preceding video frame, in order to achieve a
single GRF value that corresponds to each video frame.
Contribution of wings and hindlimbs to vertical work
Using a combination of the force-plate data and the high-speed video
recordings we estimated the percentage of the external work done against
gravity (i.e. vertical work) by the hindlimbs. The mechanics and assumptions
of this calculation are based on the methodology described by Cavagna
(1975) and are presented in
Appendix I. Briefly, we considered only the vertical components of force,
velocity and displacement during these calculations. We then compared the
amount of external work done by the bird's COM to the magnitude of the cross
product of the force measured by the force plate and the distance the COM
moved during the application of the force. The fraction of the work attributed
to the hindlimbs was estimated for all four experimental inclines (i.e.
60-90°).
The portion of the vertical work contributed by the wings was determined by subtracting the percentage of work done by the legs from 1.0. We reasoned that work was being performed either by the wings, or by the legs, and therefore the sum of the vertical work from each locomotor module must add to 1.0.
Statistics
Throughout the paper means ± standard error of the mean
(S.E.M.) are reported. Calculation of the mean and standard error
of directional data require techniques specific to this form of data in order
to overcome the mathematical problem of finding the average between the two
adjacent directions 359° and 0°. Here the standard error of the
directional data was determined by transforming the vector in question to a
unit vector with the same heading. The vector addition of all of the unit
vectors within the sample permitted determination of the mean direction. The
S.E.M. was calculated by dividing the estimated angular standard
deviation (angular dispersion) by the square root of the number of
observations (Butler, 1992).
For the accelerometer data, the mean magnitude and orientation for the six
kinematic events of interest were calculated for each recorded bout of WAIR
and climbing flight. The means for each bout were then pooled to obtain an
individual animal's mean, which were then combined to produce the reported
means ± S.E.M.
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Results |
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Accelerometry during WAIR
The trends generated from the mean values of the resultant instantaneous
acceleration measured from three birds, over nine runs and 121 individual wing
beats (Table 1, and
Fig. 3A-F). can be divided into
three temporal categories. During the first portion of the downstroke
(Fig. 3A), acceleration vectors
were generally large and oriented upwards and in the direction of travel (SDS
2.8±0.2 g, 9±15°). The second functional
division occurred during the late stages of downstroke
(Fig. 3C,D) where the
acceleration of the COM was directed towards the substrate (0.66DS
1.7±0.2 g, 111±13°). During the upstroke
period (Fig. 3E,F) the
acceleration was generally small and directed towards the ground (MUS
0.7±0.3 g, 187±24°). The standard errors
surrounding the mean orientation of the acceleration vector illustrate the
portions of the wingbeat cycle that were generally more stereotypical.
Following this criterion, the middle through late downstroke periods were the
least variable portions of the wingbeat cycle.
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Accelerometry during free flight
The mean values of the resultant instantaneous acceleration were generated
from four birds, ten flights, and a total of 57 individual wing beats
(Table 1,
Fig. 3G-L). During the early
stages of downstroke (Fig. 3G),
the acceleration vector is large and oriented upwards (SDS
2.0±0.3 g, 327±8°) in a manner consistent
with this phase of the wing beat generating much of the required lift. Through
the middle to end stages of downstroke
(Fig. 3I,J) the orientation of
the acceleration is directed parallel to the direction of travel (0.66DS
3.8±0.2 g, 72±7°), unlike during WAIR. The
upstroke portion of the wing beat (Fig.
3K,L) is characterized by small accelerations that are oriented
approximately anti-parallel to the direction of travel (MUS
0.2±0.3 g, 263±45°), suggesting that this
portion of the wing beat is not active in thrust generation. Similar to WAIR,
the standard error of the mean orientations consistently showed the late
stages of the downstroke period to be the least variable in orientation.
Force platform
Ground reaction force
The mean values of peak ground reaction force (GRF), expressed as multiples
of the individual animal's body weight (Mb) measured over
the five experimental inclines (Table
2), were all greater than those generated during fast level walks
(1.5 m s-1). These results indicate that at all of the experimental
inclines, including the vertical, chukars were able to generate large forces
against the substrate. Additionally, no decelerative phase was measured from
the parallel force axis during inclined bouts of WAIR
(Fig. 2). During level walks we
did observe a braking phase during foot contacts.
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Despite the normal axis' reduced role in weight support and vertical propulsion as incline angle was increased, the magnitude of the force exerted in the normal plane remained larger than that of the parallel axis (Fig. 4). When expressed as a fraction of the peak GRF, the lowest value measured by the normal axis was 79% of the GRF, indicating even during steep ascents the animals were applying large forces in a manner consistent with the development of traction (Fig. 5).
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Contribution of hindlimbs and wings to vertical work
During runs at 60°, an angle at which chukars generally did not engage
in WAIR, our estimate of the contribution of the hindlimbs to the external
vertical work was 98±8% (Fig.
6A). During bouts of WAIR at 70° and 80°, the estimated
contribution of the hindlimbs to the required vertical work decreased to
64±5% and 51±6%, respectively. During wing-assisted vertical
ascents we estimate the contribution from the legs to be the lowest of any of
the experimental inclines at 37±5%.
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During ascents of 60° we estimate that the wings contributed 5±2% of the observed external vertical work (Fig. 6B). During bouts of WAIR at 70°, 80° and 90°, the contribution from the wings to the observed external vertical work increased to overcome the reduction in contribution from the hindlimbs, and was 35±5%, 49±6% and 63±5%, respectively.
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Discussion |
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Accelerometers
The potential use of accelerometers in studies of locomotion has long been
recognized (Cavagna et al.,
1963; Morris,
1973
). However, their use has not been widespread
(van den Bogert et al., 1996
).
Further, published efforts focused on bird flight are limited to the single
work of Bilo and colleagues (Bilo et al.,
1985
), who mounted two accelerometers onto the ventral aspect of
the body of pigeons (Columbia liva) flying within a wind tunnel in
order to measure acceleration in the axes of thrust (horizontal plane, during
level flight) and lift (vertical plane, during level flight). These authors
did not, however, combine the thrust and lift components to determine a
resultant vector as we have done (A-P and D-V component accelerometers), and
thus the interpretation of their data is rather difficult. Our approach not
only estimates the resultant instantaneous acceleration, but also combines
these data with wing kinematics (Fig.
3) and relies heavily on the technological advances that have
occurred since the pioneering efforts of these scientists. For instance, the
use of high-speed digital video recordings, the ease of converting analog
signals to digital files, and the subsequent analysis of large volumes of
digital files, have greatly reduced the time commitment that would have been
required of the original authors.
We feel that the use of accelerometers in a manner similar to that reported here will provide functional morphologists and experimental biologists with an additional tool to investigate the timing and magnitude of biologically relevant forces. This technique is likely to be particularly appealing to those investigators who focus on modes of locomotion for which the force exerted against the environment is not easily measured (i.e. movement in a fluid). Although the technique is relatively straightforward, our results, as well as others generated under similar conditions, do not permit distinction between aerodynamic and inertial forces. Nevertheless, by incorporating detailed three-dimensional kinematics it may be possible to estimate the inertial forces and to subtract these estimates from the measured values of whole-body acceleration to determine the magnitude and direction of the resultant aerodynamic force.
Instantaneous acceleration during free flight
During free flight (Movie 1) the integration of the instantaneous
acceleration with the kinematic data revealed three general patterns. First,
the large upwardly directed acceleration during the start of downstroke
(Fig. 3A) suggests that a
phenomenon similar to the `fling' portion of the `clap and fling' mechanism
(Weis-Fogh, 1973) may
counteract the Wagner effect and allow lift production to be generated early
in the downstroke. Second, the relatively rapid decrease of the magnitude of
the acceleration vector during the late stages of downstroke
(Fig. 3D) may be caused by the
sudden transfer of momentum into the wake of the bird (i.e. the shedding of a
vortex ring). Third, during the upstroke portion of the wing beat the values
of instantaneous acceleration are only mildly directed upwards, suggesting
that the upstroke kinematics (Fig.
3F) used during these flights were only slightly aerodynamically
active. The results presented here provide empirical support for these
predictions that follow from aerodynamic theory
(Weis-Fogh, 1973
;
Spedding et al., 1984
;
Rayner, 1979c
); however, it
should be clear that inferring fluid flow would most accurately be
accomplished by the visualization of fluid dynamics (e.g. DPIV; Spedding et
al.,
2003a
,b
;
Rosen, 2003
).
Instantaneous acceleration, WAIR
The measurements of instantaneous acceleration during free flight and WAIR
suggest that the wings function differently during these two modes of
locomotion. During the majority of the downstroke the orientation of the
acceleration vectors was different between free flight and WAIR
(Fig. 3). The orientation of
the acceleration vectors measured during WAIR are towards the substrate during
the second half of the downstroke, whereas during ascending flights the
acceleration vectors are generally oriented parallel to the direction of
travel, as would be expected.
Although we are unable to address whether the forces responsible for the
observed acceleration are inertial or aerodynamic, their outcome is clear:
chukars engaged in WAIR can climb very steep inclines, including vertical
obstacles (Fig. 5). This
ability is shared with few other tetrapods, none of whom are bipeds, and those
that are capable of such precipitous ascents generally possess specialized,
derived morphological features to accomplish this task (Autumn et al.,
2000,
2002
;
Ji et al., 2002
). In contrast,
galliform species appear to co-opt existing locomotor machinery in a manner
that has only recently been appreciated. The major requirement for the use of
WAIR appears to be the animal's ability to achieve stance periods without
slipping in order to allow hindlimb propulsion. To reduce skidding on a
surface, either the normal force (also referred to as the loading force) or
the frictional coefficient between the interacting surfaces must be altered.
By incorporating WAIR into their locomotor behavior (Movie 2), chukars appear
to be adding effective weight to their hindlimbs to increase the normal
component of friction. Previously, Dial
(2003
) described how fully
volant chukars attempting to climb a smooth surface would engage in WAIR in a
futile attempt to climb even modest inclines, strongly suggesting that these
birds are committed to WAIR even though they are fully capable of flight.
These observations further suggest that the amount of effective weight that
chukar wings are capable of generating is insufficient to overcome an
experimentally reduced friction coefficient.
Hindlimb function during WAIR
Our second hypothesis asked whether the hindlimbs were active in generating
useful propulsive forces. Our measurements of peak ground reaction force
during WAIR reveal that the hindlimbs do generate sizeable forces at all of
the experimental inclines (Movie 3). Despite the decreasing trend of peak GRF
with increasing incline angle (Table
2 and Fig. 5) the
lowest value of peak GRF was 2.4 times the animal's body weight. Our estimates
of the relative contribution of the wings and hindlimbs to the total vertical
work (Fig. 6) further suggest
that these large GRFs were responsible for a substantial portion of the
required work on all inclines. The relatively low contribution (i.e. 37%) of
the hindlimbs to the total external work during vertical runs was due to the
high power requirements of these ascents rather than a dramatic decrease in
force production at this incline. The correspondingly high contribution from
the forelimbs during vertical ascents agrees well with previous results
(Dial, 2003), which
demonstrated that chukars with experimentally reduced wings were unable to use
WAIR to ascend vertical substrates, implicating the importance of wings to
ascents at these steep inclines.
When the components of the GRF were evaluated independently we did not
observe a decelerative phase in the parallel component during bouts of WAIR.
The absence of a breaking force during accelerative runs has been previously
identified in humans (Cavagna et al.,
1971) and turkeys (Roberts and
Scales, 2002
), and may represent a relatively common strategy
during activities that require high power outputs (i.e. the accelerative runs
they report, and the vertical ascents we document here).
Significance and ubiquity of WAIR
Following hatching, precocial species of birds rely almost entirely on
their hindlimbs to move rather than their as-yet-undeveloped wings (e.g.
Oken, 1837;
Starck and Ricklefs, 1998
).
Nevertheless, these animals recruit their partial wings from the first day of
hatching by flapping the forelimbs when required to negotiate even modest
inclines (Dial, 2003
).
Throughout their development, these birds use their forelimbs and hindlimbs in
combination to permit escape to elevated refuges
(Dial, 2003
). WAIR may be
common to other ground birds in general, and specifically to other similar
clades such as the tinamous of South America and the megapodes (also
galliformes) of Australia.
The strategy of employing partially grown and non-flight-capable wings to
enhance hindlimb function may also be common to altricial species of birds.
Altricial birds may use WAIR during the brief post-fledging period when these
animals are developing their aerial skills but are unable to depend entirely
upon aerial locomotion. Another opportunity for the use of WAIR is provided by
members of the Strigidae (typical owls), who are known to leave their nests
well before they are capable of flight (referred to as branching;
Marks et al., 1999); however,
details of this locomotor behavior have yet to be described. Further, the
frequency with which other altricial chicks fall from their nests and their
ability to reach the safety provided by elevated refuges such as bushes,
trees, and cliffs, are additional examples of the potential use and importance
of WAIR. Whether these animals engage in WAIR during some or any of their life
history is currently unknown, but studies of this type would represent an
exciting merger between biomechanics and natural history.
Evolutionary aspects of WAIR
For more than a century, discussions on the origin of avian flight have
been confined to the arboreal-cursorial dichotomy (i.e. tree-down
versus ground-up hypotheses). Despite volumes of publications (e.g.
Feduccia, 1996;
Chatterjee, 1997
;
Paul, 2002
) and exquisite
fossil finds (e.g. Sereno and Rao,
1992
; Zhou and Wang,
2000
; Zhang and Zhou,
2000
; Norell et al.,
2002
; Xu et al.,
2003
), few intellectual advances have been made to alter the
initial framework for either the arboreal
(Marsh, 1880
; Heilmann, 1926;
Bock, 1985
;
Rayner, 1991
;
Pennycuick, 1986
;
Norberg, 1985
;
Xing et al., 2000
) or
cursorial theses (Williston,
1879
; von Nopsca,
1907
; Ostrom,
1974
; Caple et al.,
1983
; Burgers and Chiappe,
1999
). The lack of substantial progress to resolve this impasse
may be due to the following. First, the lack of credible and incremental
adaptive transitional stages from wingless, to intermediate-winged, to
full-winged powered fliers. Second, our inability to identify plausible models
using extant taxa to reveal transitional forms employing proto-wings leading
to powered-flapping wings. And third, our failure to provide meaningful
empirical results based on living forms as models, rather than depending on
theoretical and computational models to validate either flight thesis. More
recently, an increasing number of scientists recognize the inherent difficulty
in supporting, or falsifying, the arboreal-cursorial dichotomy, and have
instead focused attention on understanding aspects of the origin of flight
that lie beyond the confines of this dichotomy (e.g.
Jenkins, 1993
;
Padian and Chiappe, 1998
;
Padian, 2001a
;
Burgers and Padian, 2001
). We
believe the present study incorporates the latter philosophy in an effort to
further advance our knowledge of the avian trajectory towards flight.
The empirical results reported here and previously
(Dial, 2003) suggest that WAIR
provides a model identifying incremental adaptive plateaus by which the
evolution of flight may have occurred. We propose that WAIR provides a logical
framework by which the proto-wings of avian precursors may have offered
adaptive benefits to their owners, despite being incapable of flapping aerial
flight. The identification of transitional stages is a crucial element towards
elucidating the trajectory leading to the evolution of complex morphological
traits (Bock, 1965
,
1985
). Despite the logical
application of WAIR to the evolution of flight, however, many questions still
remain unanswered.
The importance of WAIR to the origin and evolution of flight is clearly not
a directly testable hypothesis. Nevertheless, WAIR does demonstrate how
transitional stages of proto-wings may have been adaptive, particularly to
small bipedal cursors. Future studies that address the aerodynamic and
biomechanical requirements necessary for WAIR, such as the minimum required
wingbeat frequency, wing geometry and the potential role of ground effect,
will provide a more complete empirical picture of how proto-wings may have
functioned during the evolution of flight. Additionally, phylogenetic
analyses, based on relevant traits and states, will provide a further test of
WAIR's relevance or consistency to discussions on the evolution of flight
(Padian, 2001b).
Conclusions
Our measurements of the orientation of the whole-body acceleration vectors
and the magnitudes of the ground reaction force vectors during WAIR at steep
incline angles support our original hypothesis, that forelimb function acts to
enhance hindlimb propulsion. The reliance on this strategy by both juvenile
and adult chukars, its potential use by many other avian species, and its
possible role in the evolution of flight, all illustrate the importance of
this non-steady-state locomotor event to the life history of birds. These
non-intuitive results highlight the flexibility of the avian wing,
underscoring the importance of continued empirical investigation into the
force-generation capabilities and movements of this structure, and the
incorporation of natural animal behaviors into aerodynamic models. Moreover,
we hope our empirical results stimulate discussions and experimentation on the
origin of avian flight by supplanting the intractable arboreal-cursorial
debate with alternative, testable hypotheses. The recruitment of the
forelimbs, and the subsequent mechanics that permit chukars to run up vertical
obstacles, may also have allowed early birds to escape to elevated refuges, as
extant galliformes do, and thus provided the mechanism by which the trajectory
towards avian flight may have proceeded.
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Appendix |
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Total mechanical work on the body
The magnitude of the total external mechanical work done on the COM was
determined by:
![]() | (A1) |
![]() | (A2) |
Hindlimb external work
The magnitude of the hindlimb external work was determined by summing the
trapezoidal integral of a plot of net vertical force (net
Fv) and the displacement of the COM during force
generation (i.e. during stance on the force plate). The displacement of the
COM during force application was defined as the displacement of the COM during
the time period between touch-down on the force plate, and either toe-off from
the force plate, or touch-down of the off-foot, whichever occurred first.
To determine only the portion of the vertical force
(Fv) that was responsible for the external mechanical work
(net Fv), the portion of the vertical force responsible
for weight support was subtracted prior to the calculation of the integral.
Since it was not possible to zero the force plate with the subject animals
standing quietly on the force plate at the incline angles of interest
(Cavagna, 1975), we estimated
the portion of the Fv that was required to support the
animal's body weight (Mb). To perform this calculation two
assumptions were made. First we assumed that chukars engaged in WAIR relied
equally on their right and left feet. Second, over a period of one stride the
portion equal to weight support must average 1 x body weight. We
measured the total duration of stance from each foot during a single stride,
as well as the stride duration, and then calculated the percentage of the
stride during which foot contact was occurring (stance percentage). We then
performed the following subtraction:
![]() | (A3) |
![]() | (A4) |
![]() | (A5) |
![]() | (A6) |
![]() |
Acknowledgments |
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Footnotes |
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