JOURNAL OF MORPHOLOGY 243:173–185 (2000)
Locomotion in the Quail (Coturnix japonica):
The Kinematics of Walking and Increasing Speed
Stephen M. Reilly*
Department of Biological Sciences, Ohio University, Athens, Ohio
ABSTRACT Hindlimb segmental kinematics and
stride characteristics are quantified in several quail
locomoting on a treadmill over a six-fold increase in
speed. These data are used to describe the kinematics of
a walking stride and to identify which limb elements are
used to change stride features as speed increases. In
quail, the femur does not move during locomotion and
the tarsometatarsus–phalangeal joint is a major moving
joint; thus, quail have lost the most proximal moving
joint and added one distally. The tibiotarsus and tarsometatarsus act together as a fixed strut swinging from
the knee during stance phase (the ankle angle remains
constant at a given speed) and the tarsometatarsus–
phalangeal joint appears to have a major role in increasing limb length during the propulsive phase of the
stride. Speed is increased with greater knee extension
and by lengthening the tibiotarsus/tarsometatarsus via
increased ankle extension at greater speeds. Because
the femur is not moved and three distal elements are,
quail move the limb segments through a stride and
increase speed in a way fundamentally different from
other nonavian vertebrates. However, the three moving
joints in quail (the knee, ankle, and tarsometatarsophangeal joint) have strikingly similar kinematics to
the analogous moving joints (the hip, knee, and ankle)
in other vertebrates. Comparisons to other vertebrates
indicate that birds appear to have two modes of limb
function (three- and four-segment modes) that vary
with speed and locomotory habits. J. Morphol. 243:
173–185, 2000. © 2000 Wiley-Liss, Inc.
Although the biology of flight has seen extensive
study, terrestrial locomotion in birds has received
comparatively less attention. The allometry of avian
hind limbs (Maloiy et al., 1979; Alexander, 1983;
Gatesy, 1991a; Cubo and Casinos, 1994; Bennett,
1995, 1996) and terrestrial locomotor energetics
(Fedak et al., 1974, 1982; Pinshow et al., 1977; Bamford and Maloiy, 1980; Butler, 1991; Patak and
Baldwin, 1993) have seen considerable study. In
addition, anatomical patterns from extant birds
have been used to infer locomotor characteristics of
extinct species and to understand the evolution of
archosaur locomotion (Alexander, 1976, 1983, 1985;
Gatesy, 1990, 1991a,b, 1994; Gatesy and Middleton,
1997). Few studies, however, have focused on the
functional aspects of hindlimb locomotion in birds.
Studies of muscle anatomy (Cracraft, 1971; Rowe,
1986), motor patterns (Bekoff et al., 1975; Jacobson
and Hollyday, 1982), and muscle mechanics (Clark
and Alexander, 1975; Roberts et al., 1997) have been
used to infer muscle functions, to describe their ontogenetic development, and to establish homologies
in a few model species. Other studies have probed
the mechanics of walking and running in birds using
ground reaction forces to examine the relationship
between potential and kinetic energies during the
stride (Clark and Alexander, 1975; Heglund et al.,
1982; Muir et al., 1990). These studies have shown
that birds appear to develop kinetic patterns for
walking and running similar to those found in mammals.
Surprisingly, studies of the kinematics of terrestrial locomotion in birds have included little quantitative analysis. In the most comprehensive kinematic work to date, Gatesy and Biewener (1991)
examined speed effects on whole limb kinematics
and stride dynamics in a size series of bird taxa and
compared them to bipedal locomotion in humans.
They found that stride characteristics varied more
with animal size than speed and that small birds
exhibited a more crouched posture than larger birds.
In addition, the clear change in stride features at the
walk–run transition seen in humans was not found
in birds. While limb posture in birds clearly differs
from humans, it is unclear how their limb segments
move within a stride and when speed is increased.
Quantified kinematic profiles are limited to four
studies: Muir et al. (1990) quantify hip, knee, and
ankle profiles for slow walks in hatchling and
2-week-old chicks (speed not given); Jacobson and
© 2000 WILEY-LISS, INC.
KEY WORDS: Aves; bipedal locomotion; birds; erect posture; functional morphology; kinematics
Contract grant sponsor: Ohio University; Contract grant number:
RC 95-025; Contract grant sponsor: National Science Foundation;
Contract grant number: IBN 9727212.
*Correspondence to: Stephen M. Reilly, Department of Biological
Sciences, Ohio University, Athens OH 45701.
E-mail: [email protected]
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S.M. REILLY
Hollyday (1982) present profiles for hip, knee, and
ankle angles in the chicken; Gatesy (1994) provides
kinematic profiles for hip angle in guinea fowl moving at three speeds; and Dagg (1977) discusses ankle
kinematics in a series of birds. Additional anecdotal
data (primarily stick figures of single strides) are
presented in studies of stride characteristics, muscle
function, or force dynamics (Cracraft, 1971; Gatesy
and Biewener, 1991; Gatesy, 1994). To date, no
study has analyzed the most distal joint in the bird
limb (the tarsometatarsus–phalangeal joint) and no
study has statistically quantified the effects of speed
on segmental kinematics or accounted for interindividual variation.
In this study, I quantify hindlimb segmental kinematics and stride characteristics in several quail
locomoting on a treadmill over a six-fold increase in
speed encompassing the entire range of speed the
animals could perform. These data are used to describe the kinematics of a walking stride and to
identify which limb elements are used to change
stride features as speed increases. The results are
compared to similar data on how the limb functions
and how speed is increased in crocodilians, lizards,
mammals, and salamanders and then discussed in
relation to observations from kinetic studies. Quail
move the limb segments through a stride and increase speed in a way fundamentally different from
other nonavian vertebrates. Much of the limb acts as
a fixed strut and the tarsometatarsus–phalangeal
joint appears to have a major role in increasing limb
length during the propulsive phase of the stride. In
addition, comparisons among species suggests that
birds may have two modes of limb function that vary
with speed and locomotory habits: one involving
three limb segments and one involving four segments at higher speeds.
MATERIALS AND METHODS
One-year-old adult Coturnix japonica were obtained from the Ohio State University, Poultry Science Department, Wooster, OH, USA. Initially, 12
quail were filmed on a speed-controlled treadmill to
probe the range of speeds that the animals use. The
untrained birds moved well on the canvas treadmill
over a range of speeds up to a maximum of approximately 0.9 ms⫺1. Above this speed the animals
could not maintain belt speed. Thus, locomotory patterns were quantified over a tripling of speed within
the range for which they consistently matched
treadmill belt speed (at 0.174, 0.506, and 0.886
ms⫺1) which essentially covers the entire speed
range observed for this species on a treadmill. Although novice quail running on a treadmill for the
first time may introduce unnatural kinematic behavior, data from treadmill locomotion in chickens
has been shown to have only minor differences in
limb movements from those observed during overground locomotion (Jacobson and Hollyday, 1982).
Fig. 1. Kinematic landmarks (reflective paint dots) used to
describe limb and axial movements in quail during locomotion.
Landmarks were the eye (A), the anterolateral (B), and posterolateral (D) projections of the right side of the pelvis, the head of
the femur (C), the lateral aspects of the knee (E), ankle (F),
tarsometatarso-phalangeal (G: abbreviated as the TP joint)
joints, the tip of the middle toe (H) and a fixed point on the belt
anterior to the quail (I). Three-dimensional coordinates of these
landmarks were used to calculate the following threedimensional angles: body angle (A-C-I), pelvic angle (B-D-I), hip
angle (B-C-E), ankle angle (E-F-G), and tarsometatarsusphalangeal angle (TP angle, F-G-H).
The quantitative analyses and descriptions are
based on kinematic data for four female quail (body
masses: 118, 122, 125, 128 g). These four quail were
selected for study because they were of the same sex,
similar size, and performed well over the range of
speeds used.
Kinematic Analysis
Quail were filmed under strobe lights at 200 fields
s⫺1 using a NAC HSV-400 high-speed video system.
Elapsed time in milliseconds was recorded on each
video frame during filming. Two oblique lateral
views (roughly 45° fore and aft of lateral) of the quail
were filmed (using a mirror) during locomotion on a
70 cm long canvas treadmill. The quail ran freely on
the treadmill at most speeds, matching the treadmill speed for dozens of strides. At higher speeds,
locomotion was occasionally elicited by poking the
tail with a blunt probe. Feathers and down were
carefully cut from the rear right hindquarter of each
bird and the wing feathers were clipped to allow a
clear view of the leg. Reflective landmarks (2 mm
diameter paint dots) were painted on the skin of the
quail (Fig. 1) and the area around each landmark
was painted with black paint to accentuate the landmarks. Pelvic landmarks were painted on the anterolateral (ilium) and posterolateral (ischium) projections of the right side of the pelvis and on the skin
directly over the head of the right femur. Right
hindlimb landmarks were painted on: the knee joint
(on the anterolateral surface of the knee joint when
flexed), the ankle joint (posterolateral point of the
F1
KINEMATICS OF QUAIL LOCOMOTION
ankle (intertarsal joint) when flexed), the tarsometatarsus–phalangeal joint (lateral aspect of the
tarsometatarsus–phalangeal articulation), and the
claw of the middle toe. Except for the knee, the skin
of the quail is attached to the underlying tissues and
does not move during the step cycle. Thus, these
skin landmarks closely correspond to the underlying
skeletal landmarks. The skin on the knee moved
somewhat but close scrutiny of this landmark on
videos revealed that displacement was limited to
about 1 mm during the stride (primarily because the
knee does not move during the stride). The eye and
a fixed reference point anterior to the bird on the
treadmill were also digitized. All landmarks were
visible in both of the oblique lateral views. These
quail also had fine wire electromyographical electrodes implanted in muscles of the right hind limb in
order to record motor patterns for a parallel study of
muscle function (manuscript in preparation). The
quail were 1–3 h postanesthesia (via metathane inhalation) at the onset of filming (a period exceeding
the off-gas time for the anesthetic used, especially in
homeothermic animals).
Five strides from each of the four individuals were
selected for each of the three speeds. Strides were
selected for which the quail moved parallel to the
treadmill and matched the treadmill speed. In total,
60 strides were used in the analysis. For every other
video field for each stride (10 ms sampling) the
three-dimensional coordinates of each landmark
were digitized using stereo measurement TV
(sMTV: developed by Bruce Jayne and Garr Updegraff). Each landmark was digitized in both views
providing the three-dimensional coordinates for that
point (sMTV algorithm described in Reilly and Elias,
1998). The three-dimensional coordinate data were
then used to calculate angles from each video field to
quantify movements of the body, head, pelvis, hip,
knee, ankle, and foot through the stride (Fig. 1).
Kinematic Variables
Stride characteristics. Foot down was defined as
the first frame in which the toes hit the belt and foot
up was the first frame the toes were off the belt. The
durations of the stance phase, swing phase, and
entire stride were measured from footfall patterns
for each stride. From these, the duty factor (percent
of the stride that the foot is on the ground) was
calculated. In addition, stride length (stance duration ⫻ speed) was calculated. Limb length was calculated as the hip-to-toe distance at foot down and
foot up and knee-to-toe distance at foot down and
foot up. These two measures were used to look at
speed effects on overall limb length. Mean hip height
and mean knee height (calculated trigonometrically
as the distance of the hip (or knee) above the belt)
were computed by averaging height values for the
all stance phase frames for each stride. For comparisons to other studies, normalized velocities were
175
calculated for each individual at each speed using
the Froude number (Alexander and Jayes, 1983):
velocity2/g (gravitational acceleration constant [9.8
ms]) * h (hip height). The Froude number was also
calculated because it can be used to estimate
whether an animal is mechanically running (a “kinetic run”: potential and kinetic energies are in
phase) or walking (a “kinetic walk”: potential and
kinetic energies are out of phase). The mechanical
transition from a kinetic walk to a kinetic run occurs
at Froude numbers between 0.36 and 0.64 across
vertebrates studied (Alexander and Jayes, 1983).
Because the femur did not move during locomotion,
both hip and knee height were used for h in the
Froude number calculations.
Limb and pelvic movements. To quantitatively assess the effects of speed on hindlimb kinematics, a
series of angular and timing variables were taken
from profiles for each stride to describe and statistically compare movements of the body, pelvis, and
hindlimb joints in three-dimensional space. The
variables were chosen to capture the minimum and
maximum excursion angles (and associated timing)
of the body, pelvis, and each of the four major joints
of the hindlimb (the hip, knee, ankle, and tarsometatarsus–phalangeal joint, hereafter termed the
TP joint) as shown in Figure 1. For all joints extension means an increase in joint angle and flexion
means a decrease in joint angle.
The angles of the body, pelvis, and each limb joint
(Fig. 1) were measured at the time of right foot down
and foot up. These angles indicate the positions of
the body and limb joints at the beginning and end of
the stance phase. The rest of the angular variables
quantified the minima and maxima of each joint
profile and excursions between them (when present:
the body angle, pelvic angle, and hip angle did not
change, so no further variables were taken for these
features). For knee movements, the minimum angle
(in early swing phase), maximum angle (coincident
with foot down) and angular excursion (during
swing) were measured (see Fig. 3). For the ankle
movements, the point at which the ankle angle begins to decrease (termed “angle at ankle drop off,”
which occurred at about foot up), its minimum
(about mid-swing), and excursion (during swing)
were measured. TP angle minimum (at about midstance), maximum (at about foot up), and excursions
(during stance and swing) were also measured.
Timing variables were taken to describe the timing of the minima and maxima of the joint movements (the times to the various joint angles described above) and the durations of the joint
excursions described above. All timing variables
were taken relative to time 0 at right foot down. For
comparisons across speeds, timing variables (all except for one swing-phase feature, ankle minimum)
were scaled to the stance duration for each stride
(variables expressed as a percentage of stance duration). This was done so that the timing of kinematic
176
S.M. REILLY
events occurring during the stance phase are compared relative to the stance phase (when locomotory
forces are conveyed to the substratum) and are not
confounded by differential changes in the stance and
swing phases with speed (Reilly, 1998). Minimum
ankle angle was the only variable clearly occurring
during the swing phase and, thus, it was scaled to
swing phase duration ((time to ankle minimum stance duration)/swing duration) because the swing
phase did not change with speed.
Statistical Analyses
To describe the gaits used by the quail, the timing
of footfalls was measured for both feet for each stride
(for a complete cycle for each of the two feet) and an
overall mean gait diagram for one individual was
plotted using mean footfall timing values for five
strides for each of the speeds and postures. To
graphically illustrate and compare movement patterns of the body and hindlimb joints for each speed,
mean kinematic profiles were generated for one individual. Mean angles (⫾1 SEM) for five strides
from each speed were plotted with strides aligned by
treating the time of right-foot down as time zero
with mean profiles scaled to stride duration.
Kinematic variables were statistically compared
using a repeated measures analysis of variance
(ANOVA) with speed as the main effect (testing the
effects of a six-fold increase in speed). Because all
individuals serve in all three speed treatments, this
analysis employs a pure within-subjects (repeatedmeasures) design (Zolman, 1993). This repeated
measures design (performed using Systat威 version
6.0) has the advantage of testing differences in the
main effect after variation among individuals,
within individuals within behaviors, and residual
error have been extracted. The a priori choice to use
the same individuals in all of the treatment combinations was made to control for the problem of interindividual variation because the within-subjects
design provides a more conservative test for significance than standard ANOVA tests (because the
F-ratio for the main effect is calculated by dividing
the mean square by the interaction mean square
rather than the error mean square). All ANOVAs
run had degrees of freedom of 2 (3 speeds ⫺1) and 6
(3 speeds ⫺1 ⫻ 4 individuals ⫺1). Given the more
conservative design, an alpha level of 0.05 is considered to be sufficient to indicate statistical significance even with multiple univariate comparisons
within limb joints. The ANOVA was not performed
for the body angle variable because data were variably missing when the eye landmark was out of view
and because there were no obvious speed differences
based on the means.
RESULTS
Representative video frames portraying a single
stride of the right hindlimb during a walk are shown
Fig. 2. Lateral and dorsal images from high-speed video illustrating one walking stride of Coturnix japonica moving at 0.506
ms⫺1. Time is indicated on each frame in milliseconds from foot
down (time 0) to the subsequent foot down (295 ms); foot up is at
220 ms. White dots on images are landmarks used to acquire
kinematic data.
in Figure 2. Means (pooled across individuals) and
ANOVA results for stride and limb data are presented in Table 1. Mean kinematic profiles for the
angular movements of the pelvis and hindlimb joints
of one individual are presented in Figure 3. Means
for angular and (scaled) timing variables (pooled
across individuals) are presented in Table 2, with
ANOVA results comparing speed effects on these
variables in the right-hand column. Based on
Froude numbers (Table 1), the first two speeds were
kinetic walks while the high speed would be considered a kinetic run.
Kinematics of a Walking Stride
The general patterns of hindlimb, body, and pelvic
movements were similar across speeds in the quail
(Fig. 3); therefore, the kinematics of a walking stride
are described below based on the data for the middle
speed of 0.506 ms⫺1, which is interpreted to be a
kinetic walk based on Froude number (Table 1).
F2
T1
F3
T2
KINEMATICS OF QUAIL LOCOMOTION
177
TABLE 1. Stride characteristics (means ⫾ S.E.M.) and analysis of speed effects in quail locomoting at three speeds
Speed
effect
Speed
Variable
Stance duration (ms)
Swing duration (ms)
Stride duration (ms)
Duty factor
Stride length (cm)
Mean hip height during stance (cm)
Mean knee height during stance (cm)
Limb length at down (cm)
Limb length at up (cm)
Knee to toe length at down (cm)
Knee to toe length at up (cm)
Froude number
Froude number (knee)
0.174 ms⫺1
0.506 ms⫺1
0.886 ms⫺1
(P)
396 ⫾ 10
94 ⫾ 4
491 ⫾ 10
0.80 ⫾ 0.01
7.2 ⫾ 1.5
9.4 ⫾ 0.1
6.2 ⫾ 0.2
11.5 ⫾ 0.7
9.3 ⫾ 1.1
6.4 ⫾ 0.8
7.2 ⫾ 0.6
0.023 ⫾ 0.001
0.034 ⫾ 0.001
210 ⫾ 3
79 ⫾ 2
289 ⫾ 3
0.73 ⫾ 0.01
14.6 ⫾ 1.4
9.3 ⫾ 0.1
6.2 ⫾ 0.1
11.7 ⫾ 0.8
9.0 ⫾ 0.5
6.6 ⫾ 0.2
7.6 ⫾ 0.4
0.28 ⫾ 0.01
0.42 ⫾ 0.01
133 ⫾ 1.5
72 ⫾ 3
205 ⫾ 3
0.65 ⫾ 0.01
18.2 ⫾ 2.5
9.3 ⫾ 0.1
6.4 ⫾ 0.1
12.2 ⫾ 0.4
9.3 ⫾ 0.4
7.6 ⫾ 0.5
8.1 ⫾ 0.7
0.86 ⫾ 0.01
1.23 ⫾ 0.03
⬍0.001*
0.114
⬍0.001*
0.003*
⬍0.001*
0.408
0.124
0.002*
0.244
0.004*
⬍0.001*
Means are pooled for four individuals (n ⫽ 5 strides each, total n ⫽ 20 per speed).
Significant speed effects are indicated by an asterisk (P ⬍ 0.05).
Movements are described relative to the stride and
footfall patterns (Table 1; Fig. 3) and based on the
mean kinematic profiles illustrated for one individual (Fig. 3: open squares) and the mean angular and
timing data pooled for all three individuals at the
middle speed (Table 2). Statistically significant differences indicating speed effects (Table 2) are described in the subsequent sections.
During locomotion at 0.506 ms⫺1, body angle remained at 23–25° while the pelvic angle remained
45– 48° (both angles relative to the fixed belt landmark), indicating that the pelvis and body remained
stable throughout the stride. The hip angle did not
change either, remaining at approximately 80° from
the pelvic axis, indicating that the femur was held
stationary during the stride. Hip and knee height
remained at approximately 9.3 and 6.2 cm, respectively, throughout the stance phase.
Maximum extension of the knee of approximately
114° occurred at foot down. The knee was flexed at a
uniform rate to its maximum flexion of 53° at approximately 98% of stance duration. The knee then
rapidly reextended to its fullest extent during the
swing phase. The ankle was at its maximum extension (of about 110°) at foot down and remained at its
maximum until it began to flex at about 86% of
stance phase. The ankle appears to extend slightly
during mid-stance (Fig. 3) but the angle at foot down
and just before it begins to flex are not significantly
different (Table 2). Once ankle flexion begins, it continues to its minimum flexion point of 48° in the
middle of the swing phase. It then extends rapidly to
its maximum again at foot down. The TP joint gradually flexes, then extends during the stance phase.
From 159° at foot down the TP angle decreases to
117° at 55% of stance phase. It then increases 52° to
its maximum of 169° just before foot up (at 98% of
stance phase). The TP joint is then rapidly flexed
early in swing phase to pick up the digits and then
extended again prior to the next foot down.
Speed Effects
Gait and stride characteristics. Mean gait diagrams for both postures and speeds are illustrated
in Figure 4. The quail used a bipedal gait with the
body supported by a single foot only during the middle third to half of the stance phase. The duration of
stance phase and total stride time decreased significantly with increased speed, while the swing duration did not change (Table 1). The mean percentage
of the stride that the right foot is on the substratum
(duty factor) decreased significantly (from 80 to
65%) with the three-fold increase in speed (Table 1).
The opposite foot was off the ground during approximately the middle third of stand phase and increases to about the middle half as speed increased
(Fig. 4). Stride length increased significantly with
speed (from 7.2 to 18.2 cm). Thus, the quail increase
speed by moving the limb faster and farther. The
height of the hip above the treadmill did not change
significantly remaining at approximately 9.3 cm
during stance phase for all three speeds (Table 1).
Limb segment kinematics. Significant speed effects were found in only six kinematic variables and
these involved angular movements in only the knee
and ankle joints (Table 2). The maximum knee angle
(which occurs at foot down) increased significantly
(approximately 20°) with speed. Because the minimum knee angle did not change, this increase in
knee extension is produced by a significant increase
in knee excursion from its minimum to maximum
during the swing phase. This indicates that the knee
is extended more at foot down but not retracted
more as speed increased. Because the stance duration decreased with speed and the relative timing of
knee movements did not change, the knee joint must
be moving faster as well.
The ankle exhibited significant increases in the
angle at foot down, the angle at drop-off, and minimum ankle angle (Table 2), and each of these in-
F4
178
S.M. REILLY
Figure 3
KINEMATICS OF QUAIL LOCOMOTION
179
TABLE 2. Angular and timing variables and speed effects for body and hindlimb joint movements in quail
locomoting over three speeds
Speed
⫺1
Variable
0.147 ms
1
Body angle at down
Body angle at up1
Pelvic angle at down
Pelvic angle at up
Hip angle at down
Hip angle at up
Knee angle at down
Knee angle minimum
Time to knee minimum
Knee angle excursion
Ankle angle at down
Ankle angle at drop off
Time to ankle drop off
Ankle angle minimum (swing)
Time to ankle minimum (swing)
Ankle angle excursion
TP angle at down
TP angle minimum
Time to TP angle minimum
TP angle maximum
Time to TP angle maximum
TP angle excursion stance
TP angle excursion swing
25 ⫾ 1
24 ⫾ 2
49 ⫾ 2
49 ⫾ 2
77 ⫾ 3
78 ⫾ 3
99 ⫾ 2
50 ⫾ 2
390 ⫾ 12
(0.98 ⫾ 0.01)
51 ⫾ 3
96 ⫾ 2
98 ⫾ 2
343 ⫾ 6
(0.87 ⫾ 0.02)
35 ⫾ 2
428 ⫾ 11
(0.32 ⫾ 0.05)2
58 ⫾ 2
162 ⫾ 1
118 ⫾ 2
234 ⫾ 5
(0.60 ⫾ 0.02)
171 ⫾ 1
384 ⫾ 12
(0.97 ⫾ 0.02)
44 ⫾ 2
53 ⫾ 2
Speed effects
⫺1
0.506 ms
23 ⫾ 4
25 ⫾ 3
48 ⫾ 1
45 ⫾ 1
79 ⫾ 2
83 ⫾ 2
114 ⫾ 2
53 ⫾ 2
205 ⫾ 4
(0.98 ⫾ 0.01)
63 ⫾ 2
110 ⫾ 1
111 ⫾ 2
181 ⫾ 3
(0.86 ⫾ 0.02)
48 ⫾ 2
247 ⫾ 4
(0.35 ⫾ 0.03)2
63 ⫾ 2
159 ⫾ 2
117 ⫾ 2
105 ⫾ 4
(0.55 ⫾ 0.02)
169 ⫾ 1
206 ⫾ 2
(0.98 ⫾ 0.01)
42 ⫾ 2
52 ⫾ 2
0.886 ms
⫺1
22 ⫾ 3
23 ⫾ 3
52 ⫾ 1
48 ⫾ 2
78 ⫾ 1
78 ⫾ 1
122 ⫾ 2
53 ⫾ 1
144 ⫾ 3
(1.08 ⫾ 0.02)
70 ⫾ 2
116 ⫾ 2
117 ⫾ 2
126 ⫾ 3
(0.95 ⫾ 0.02)
54 ⫾ 2
175 ⫾ 3
(0.42 ⫾ 0.03)2
63 ⫾ 3
158 ⫾ 1
111 ⫾ 2
79 ⫾ 3
(0.59 ⫾ 0.03)
166 ⫾ 1
142 ⫾ 3
(1.07 ⫾ 0.03)
48 ⫾ 3
56 ⫾ 3
(P)
0.583
0.521
0.950
0.519
0.012*
0.616
0.095
0.014*
0.007*
0.011*
0.117
0.002*
0.150
0.318
0.104
0.087
0.275
0.102
0.267
0.207
0.654
1
N’s are variable because of eye landmark being off screen in some runs, ANOVA not done.
Ankle minimum occurs during swing phase and is scaled to swing duration.
* Significant speed effect at 0.05 alpha level.
Means (⫾ SEM) for each speed (n ⫽ 20) are pooled for four individuals (n ⫽ 5 strides each).
Angular variables are in degrees. Timing variables are given in real time in milliseconds and scaled to stance duration (in
parentheses).
TP ⫽ tarsometatarsus-phalangeal joint.
2
creased approximately 20° with increasing speed
(Table 2). This indicates that the ankle is moved
through the same kinematic pattern but is shifted to
a more extended position as speed increases. Speed
had no effect on the relative timing of ankle movements or any of the hip, pelvic, and body movements.
Fig. 3. Mean profiles for body and right hindlimb joint kinematics (in degrees) for Coturnix japonica moving at three speeds
(open circles ⫽ 0.174 ms⫺1, squares ⫽ 0.506 ms⫺1, circles ⫽ 0.886
ms⫺1). Angular means ⫾ SEM are shown for five strides from one
individual. The x axis indicates time as percent stride duration
beginning at right foot down (time 0). The body and pelvic angles
are relative to a fixed point on the treadmill anterior to the quail.
The remaining angles are the actual joint angles and, thus, decreasing angles indicate flexion while increasing angles indicate
extension of a given joint. The vertical lines on each plot indicate
the mean times for the end of the stance phase (foot up) of 65, 73,
and 80% for the high, medium, and low speeds, respectively.
Significant differences between speeds are based on ANOVA results given in Table 2.
DISCUSSION
Segmental Components of Hindlimb
Movements During Locomotion
At all three speeds studied, the hip joint remains
fixed with the femur in an anteroventral position
about 80° below the axis of the pelvis, which equates
to about 45° below the direction of movement (Fig.
2). Thus, the knee joint is the effective point from
which the remaining limb segments rotate relative
to the body. During swing phase the distal portion of
the limb as a whole is lengthened prior to foot down
by extending all three distal joints (knee, ankle, and
TP) with the knee having the greatest effect because
of its longer lever arm (the tibiotarsus is about 1.3
times longer than the tarsometatarsus) and longer
time of extension.
Throughout the stance phase the knee is flexed,
the ankle remains static (until the last 10% of
stance, when it begins to flex), and the TP joint
flexes then extends. Because the ankle joint remains
essentially static, the tibiotarsus and tarsometatarsus together act as a rigid strut and the TP joint
180
S.M. REILLY
Fig. 4. Mean gait patterns (scaled to stride duration) based on
footfall timing of both hindlimbs from one quail moving at three
speeds (n ⫽ 5 for each). Note the essentially identical gait pattern
and lack of an aerial phase exhibited by all three speeds. L, left
side; R, right side; H, hindfoot; F, forefoot.
swings in an arc relative to the knee. Because the
foot is placed cranial to the knee at foot down, knee
flexion moves the TP joint in an arc that reaches a
point directly below the knee after foot down and
then the position of the joint swings posterodorsally
off the substratum during the rest of the stance
phase (the movement arc reaches bottom dead center and then swings toward the tail). From reviewing foot contacts on the videos it appears that the
digits are extended below the TP joint at foot down
(see Fig. 2 Time 0 and 295) and are then flattened
onto the belt by the time the TP joint reaches bottom
dead center under the knee. The TP joint continues
to flex through the first half of stance as it is rotated
posteriorly. Then the TP joint begins to extend (rolling the bird onto the anterior digits). Thus, the extending digits add to the effective limb length and
make up for the loss of effective limb length due to
the dorsocaudally rotating TP joint. A slight (but
statistically insignificant) increase in ankle angle
during the late stance is evident in the higher
speeds in quail (Fig. 2) and has been observed in
chickens and pigeons (Cracraft, 1971; Jacobson and
Hollyday, 1982). This may be occurring to extend the
limb somewhat as the TP arc swings up and away
from the ground. Late in stance phase the ankle
begins to flex, which may contribute to stiffening the
TP joint in order to roll the weight onto the digits
just prior to foot up. During the swing phase the TP
joint begins to flex at foot up and this, combined with
continued flexion of the ankle, rapidly elevates the
TP joint and digits (which are not extended beyond
180° during stance). All three joints are then extended to place the foot down for the next stride.
In sum, the distal limb must compress, then extend during the stance phase because the knee and
hip heights do not change. Limb compression during
the first half of stance is accomplished by flexing the
knee and the TP joint, while extension of the limb in
the second half of stance is done, in spite of continuing knee flexion, by extending the TP joint and, at
higher speeds, with some extension of the ankle.
Mechanisms of limb retraction. Knee flexion has
been considered the primary motive force in retracting the limb in small birds (Cracraft, 1971; Jacobson
and Hollyday, 1982; Muir et al., 1990; Gatesy and
Biewener, 1991). Electromyographical data for the
primary knee flexor in chickens (the iliofibularis:
Jacobson and Hollyday, 1982) show that it has a
large burst of activity during mid-stance almost exactly coincident with the time the opposite foot is off
the ground (Fig. 4) and during which time the knee
goes through about half of its flexion. During this
time, the quail data show the TP joint at its minimum flexion (at 55– 60% of stance). Thus, the TP
joint cannot be involved in limb extension at this
time but some energy storage may occur in tendons.
These two observations seem to be good evidence
that knee flexion is clearly a key component in retraction of the limb (but see below). The ankle does
not appear to contribute to limb length changes because it remains static for the first 90% of stance and
then only flexes. Later in the stance, the continued
flexion of the knee and the onset of ankle flexion will
shorten the limb. This is when extension of the TP
joint appears to have an important role in increasing
limb length. These novel data on the TP joint in
quail are the first to suggest that this joint may aid
in propulsion via extension of the digits late in
stance.
Segmental movements in relation to fore–aft
ground reaction forces. In both quail (Clark and Alexander, 1975; Heglund et al., 1982) and chickens
(Muir et al., 1990) braking (decelerating) fore–aft
forces shift to caudally directed (accelerating or propulsive) fore–aft forces beginning at about 50% of
stance phase and these propulsive fore–aft forces
appear to peak during the last fifth of the stance
phase. The beginning of propulsive (accelerative)
forces at mid-stance suggests that knee flexion may
produce some propulsion at this time but the observation that accelerative forces are greatest in the
last fifth of stance (when TP joint extension is occurring and the knee flexion is effectively shortening
the limb) suggests that the TP joint must contribute
significantly to propulsion.
Comparisons of Limb Segment Mechanics
in Other Species
The kinematic patterns described above are similar
to the few other data available on hip, knee, and ankle
kinematics in birds (domestic pigeon: Cracraft, 1971;
domestic chicken: Jacobson and Hollyday, 1982;
hatchling chicks: Muir et al., 1990; and anecdotal data
for Coturnix japonica: Clark and Alexander, 1975). All
of these species have continuous knee flexion during
stance. The static ankle angles I observed during the
stance in quail are also seen in chickens running on a
treadmill and, in fact, Jacobson and Hollyday (1982)
proposed that the tibiotarsus–tarsometatarsus acts as
a strut based on activity of ankle muscles. Pigeons and
KINEMATICS OF QUAIL LOCOMOTION
181
Fig. 5. Comparative kinematics of limb segments in
vertebrates. Mean profiles for
the proximal, middle, and distal joints in a quail (E, this
study), an alligator (}, Reilly
and Elias, 1989) and a lizard
(■, Reilly and DeLancey,
1997b) are presented scaled to
stance duration. Because the
hip joint does not move in the
quail, the proximal moving
joint is the knee, the middle
joint is the ankle, and the distal joint is the TD joint. These
are contrasted with the hip,
knee, and ankle joints, respectively, in the other two species.
Note the basic similarity of the
kinematics of joints at the
same position. The quail knee
profile has been converted to
reflect the movement of the
tibiotarsus relative to the body
axis for comparison to similar
movements of the proximal
joints in other vertebrates.
F5
younger chickens and many other birds, however, do
appear to have some ankle flexion during the midstance phase in studies where birds run overground
past the camera (Cracraft, 1971; Dagg, 1977; Muir et
al., 1990).
The most striking feature of quail locomotion is
that they essentially do not move the femur during
locomotion. An essentially static hip joint during
walking has been reported for the above species and
guinea fowl (Gatesy, 1994). Having immobilized the
hip joint these birds maintain three moveable limb
joints by adding the TP articulation as a major moving joint. Comparative data for TP joint movements
are not available but based on my data for the quail
there is an interesting shift in joint kinematics in
walking birds to match the kinematics of the three
more proximal joints used by other vertebrates.
Figure 5 presents comparative limb kinematics
for the three most proximal moving joints in a variety of diapsids. When the patterns of hindlimb
movement for each of the three proximal most joints
(the hip, knee, and ankle) of lizards (which are similar to salamanders and mammals; Vilensky and
Gankiewicz, 1990; Ashley-Ross, 1994a; Reilly and
DeLancey, 1997a,b) and alligators (Reilly and Elias,
1998) are compared to the patterns for the first three
proximal most joints in the quail (the knee, ankle,
and TP joints), similar general patterns are ob-
served for each joint (for comparison, quail knee
angles [the proximal moving joint] have been adjusted to reflect movements of the tibiotarsus relative to the body axis: measured as the angle between
the tibiotarsus and the body axis). Because the proximal joint has a static articulation point on the body,
it has a single cycle of movement, swinging the appropriate limb bone from anterior to posterior during stance and returning it during the swing phase,
and is essentially identical in all these species. The
middle and distal joints exhibit biphasic patterns,
flexing and extending during both the stance and
swing phases except in the archosaurs. Quail and
alligators hold the middle joint static during the
stance (although recall that some birds show some
flexion of the middle joint (the ankle) during midstance, like the mammal, salamander and lizards).
In the distal joint all taxa displayed a biphasic pattern of flexing and extending the joint during both
the stance and swing phases. Even though different
sets of joints are used these patterns fit surprisingly
well the idealized joint profiles predicted on the basis of achieving the least instantaneous total positive power of leg musculature in each joint throughout the stance (Kuznetsov, 1995). The archosaurs,
however, fit the Kuznetsov model best and seem to
share the novel static middle-joint kinematics during stance.
182
S.M. REILLY
Because the hip does not move in quail and the
knee is the effective proximal end of the limb, it
makes use of the traditional femur/tibia ratio (Gregory, 1912) problematic as a comparative indicator of
cursoriality. Gatesy and Middleton (1997) have
shown this ratio to be of little value in describing
speed patterns in birds and suggest that the tarsometatarsus must be included in the evaluation of
basic limb design in birds. In quail, the immobile hip
illustrates the futility of using this ratio and the
importance of the TP joint on the stride demonstrates the importance of the tarsometatarsus and
its interaction with the phalanges in limb function
in birds.
Speed Effects
Stride and gait characteristics. As vertebrates
increase speed, both the stance and swing durations
decrease through a range of walking speeds until the
swing phase reaches its minimum duration. At
higher speeds the stance duration continues to decrease until some other factor is used to further
increase speed (such as a gait change). Thus, it is
fairly universal in vertebrates (e.g., Wisleder et al.,
1990; Gatesy and Biewener, 1991; Ashley-Ross,
1994b; Reilly, 1998) to see swing duration decrease
as speed increases from very slow speeds. The quail
in this study, however, had no changes in swing
phase duration over the six-fold increase in speed
from the slowest to the fastest speed they would
move on a treadmill. Gatesy and Biewener (1991)
have also shown a constant swing phase over slow
speed ranges (⬍1 ms) in bobwhite quail, and in this
regard quail appear to be different not only from
other birds analyzed (Gatesy and Biewener, 1991),
but other vertebrates as well.
As the quail increased speed their gait patterns
remained essentially the same (Fig. 4) and duty
factors decreased but remained well over 50%. This
matches other observations that small birds do not
use a terrestrial gait with an aerial phase (Cracraft,
1971; Gatesy and Biewener, 1991) even though as
speed increased there was a trend toward having a
longer period of single foot support during the middle of stance phase (Fig. 4).
Limb segment kinematics — increasing
stride length. Given that stride length increased
significantly as speed increased, how is it that the
quail attained longer strides? The kinematic analysis revealed that hip joint movements had nothing to
do with increasing speed over this range of speeds
and the relative timing of joint angle excursions did
not change during the stance phase. Greater stride
lengths were attained by simple changes in the knee
and ankle kinematics. The maximum knee angle at
foot down increased approximately 20° over the
speed range but the minimum knee angle did not
change. Thus, the overall knee excursion increased
about 20° solely by extending the knee farther dur-
ing the swing phase. As speed increased the ankle
shifted to a consistently greater angle (but fixed at a
given speed) over most of the stance phase, increasing approximately 20° over the speed range. So as
speed increases the limb is extended more anteriorly
at foot down by increasing knee and ankle extension
and the limb is extended more posteriorly at foot up
with a greater ankle angle at higher speeds. The TP
joint did not show an increase in excursion with
speed, as might be expected if it has a major contribution to propulsion, as it does in alligators (Reilly
and Elias, 1998) and some lizards (Fieler and Jayne,
1998). However, it may be that extending the limb
via knee and ankle extension does not necessarily
require a change in the relative timing and extent of
TP joint movement as speed increases, especially if
the relative timing of late stance events do not
change.
Because hip height and knee height did not
change during the stance phase (Table 1), greater
extension of the ankle and knee at foot down and
the greater ankle extension at foot up would have
to result in a greater anterior and posterior placement of the foot during the stride. This is reflected
in the significant increase in limb length and
knee-to-toe length at foot down (of about 1 cm) and
the significant increase in knee-to-toe length at
foot up (of about 1.6 cm, Table 1). Note that the
knee-to-toe distance better characterizes the
length of the effective limb because the hip and
knee do not move. This indicates that the increase
in limb retraction was greater than protraction.
This pattern fits well with data on bobwhite quail
but is in contrast to estimates of limb excursion
movements in other birds and humans, which
show that increases in overall limb excursion with
speed are due only to a greater degree of retraction
(Gatesy and Biewener, 1991: fig. 8).
Comparisons to other species. Several recent
quantitative kinematic analyses of speed effects on
hindlimb kinematics in walking vertebrates facilitate a gross comparison of components of the hindlimb that are used to increase speed. Speed effects
for the quail can be compared to walking in those for
a salamander (Dicamptodon tenebrosus: AshleyRoss, 1994b), two mammals (Canis familiaris: Goslow et al., 1981; Felis cattus: Goslow et al., 1973;
Grillner, 1975, 1981; Halbertsma, 1983), two lizards
(Sceloporus clarkii: Reilly and DeLancey, 1997a,b;
Dipsosaurus dorsalis: Fieler and Jayne, 1998), and
alligator (Reilly and Elias, 1998). Although these
studies differ in speed ranges, limb postures, and
types of kinematic data, some comparison of walking
joint movements can be made. The salamander differs from the others in using pelvic rotation as a
component to effect greater limb movements. One
pervasive pattern across all these species is that the
amount of femoral excursion does not change with
speed, but rather the femur is either retracted faster
through the same basic range of retraction. In the
KINEMATICS OF QUAIL LOCOMOTION
more sprawling vertebrates (D. tenebrosus and S.
clarkii) and mammals this appears to be the primary mechanism to increase speed. The semi-erect
vertebrates (D. dorsalis and alligator) employ more
distal limb joints to effect increases in speed by
increasing knee extension to increase limb length
throughout the stance phase, and by increased extension of the ankle during late stance phase. In
terms of anatomically homologous joints the quail is
consistent with the semi-erect species in using the
distal joints (knee and ankle) to increase speed but it
does it in a different way: both hip and ankle joints
remain static during the stance at a given speed
(with greater knee and ankle extension used to increase limb length during the stance phase as speed
increases). In terms of analogous moving limb segments, the quail is different from the other vertebrates in increasing the range of excursion of the
proximal-most moving joint (the knee), keeping the
middle joint (ankle) static, and showing no change in
the kinematics of the distal joint (TP) during stance
as speed increases. Thus, in terms of speed effects
quail limb kinematics have very little in common
with quadrupedal vertebrates whether anatomically
homologous or analogous moving segments are compared. Whereas quail are similar to humans in that
the most proximal movable joint provides the primary joint displacement by which the body is moved
forward, the maximum extension of the first segment at foot down is only 120° in quail compared to
nearly 180° in humans and the distal joints of quail
are strongly bent during the stride. Thus, the quail
limb is greatly compressed throughout the stride
and has been suggested to be more compliant to
increase stability of the body and allow the head to
remain stable (Gatesy and Biewener, 1991) as in
human “groucho walkers” (McMahon et al., 1987). In
addition, it has been shown that the degree of quail
hindlimb extension is modulated to maintain constant hip height during steps on heterogeneous and
unpredictable substrates (Clark, 1988, cited in
Gatesy and Biewener, 1991). The use of limb compliance to maintain a constant body position in quail
should come at a cost in terms of the bending strain
on limb segments that are held relatively perpendicular to the ground reaction forces on the limb, especially in the femur (Gatesy, 1991a). Perhaps hip
muscles are stabilizing the femur to reduce strain,
as evidenced by the activity in a series of hip antagonists during the stance in chickens (Jacobson and
Hollyday, 1982).
Adding Femoral Movements to Afford
Higher Groundspeed?
Quail and other birds do not appear to use femoral
retraction to any appreciable extent while moving at
speeds of up to 2 ms⫺1, which is the maximum
ground speed attained by smaller birds (Cracraft,
1971; Jacobson and Hollyday, 1982; Gatesy and Bie-
183
wener, 1991). Larger birds that can increase speeds
to over 8 ms⫺1 begin to use femoral retraction at
about 2 ms⫺1 and increase femoral retraction considerably at higher speeds (Gatesy and Biewener,
1991; Gatesy, 1994). Information on the kinematic
changes in distal joints when femoral retraction begins are not available to address the very interesting
question of how distal joint kinematics change when
the onset of femoral retraction adds a fourth joint to
the limb at higher speeds. Smaller birds may be
ecologically or behaviorally adapted to walk up to a
certain speed and then fly, instead of changing gaits
to a run. Larger birds appear to be more predisposed
to change gaits and run to higher speeds and avoid
flying. This pattern would fit with energetic patterns
of size effects on the costs for running and flying.
Because the cost of terrestrial locomotion is six
times greater in a quail-sized bird (0.1 kg) compared
to a turkey-sized bird (5 kg) and the cost of level
flight in a quail-sized bird is about three times less
than the cost in a turkey-sized bird (Tucker, 1970),
small birds may save energy by switching to flying
and bigger birds may actually avoid flying in favor of
running to higher speeds to save energy.
Relating Kinematics to Kinetics in Quail
Based on mean duty factor data reported here, the
gait at all three speeds is categorized as a walk
according to the terminology of Hildebrand (1985),
which defines a run as a foot-fall pattern involving
an aerial phase. Kinetic definitions of the walk and
run (often called a trot) are based on patterns of
kinetic and potential energy fluctuations during
stride being out of or in phase, respectively (Cavanga et al., 1977). Alexander and Jayes (1983)
present a third way of identifying the walk–run
transition based on normalization for size differences based on the hip height and velocity using the
Froude number. The walk–run transition is supposed to occur at approximately between Froude
values of 0.36 – 0.64. Although data for one method
of defining gaits are commonly converted to another,
the correlation of these three methods of defining
the walk–run transition has not been well studied.
Gatesy and Biewener (1991) show the kinetic walk–
run transition point is particularly difficult to discern in smaller birds using foot-fall patterns. They
showed that bobwhite quail running at 2 ms⫺1 had a
Froude number of 4.32, which is well over the 0.36 –
0.64 cutoff for the walk–run transition based on
Froude number, and yet the quail still did not have
an aerial phase. Published kinetic data for quail are
also problematic in identifying the walk–run transition. Force records for kinetic walks typically have
two peaks of vertical force, corresponding to a pulse
of deceleration followed by a pulse of acceleration
seen during foot-fall, while kinetic runs have a single vertical force peak during the stance phase (Cavagna et al., 1977; Alexander, 1980). Muir et al.
184
S.M. REILLY
(1990) clearly show these patterns and expected energy phase relationships for a walk and run in the
hatchling chicks at Froude numbers of 0.14 and
0.81, respectively, which nicely spans the 0.36 – 0.64
Froude number walk–run transition zone. Heglund
et al. (1982) show clear kinetic runs in Chinese
painted quail (Excalfactoria chinensis) at speeds of
1.04 and 1.75 ms⫺1. However, a force record for
Japanese quail (Clark and Alexander, 1975) shows a
kinetic walk force pattern (two peaks of vertical
force) with kinetic run energy phase relationships
(potential and kinetic energy in phase) at a speed of
0.5 ms⫺1 and Froude number of 0.36. Here the
speed, Froude number, and force profile indicate a
walk, but the calculated energy fluctuations indicate
a kinetic run. By contrast, either the energy calculations are amiss in Clark and Alexander (1975) or
there is something peculiar about limb compliance
in Japanese quail. In addition, kinetic walks, which
involve reversed pendulum-like limb motions, usually have a rise in hip height at mid-stance while
kinetic runs, which employ a more spring-based
limb system, have a dip in hip height during the
stance phase (Alexander, 1980). The quail in the
present study had constant hip and knee heights
(Table 1) for both the lower speed that can be inferred to be kinetic walks (Froude numbers with hip
or knee ⬍0.43) and the higher speed inferred to be
kinetic run (Froude number ⫽ 0.86 [hip], 1.23
[knee]). Although the highest speed may be a kinetic
run, it had no significant kinematic differences from
the walks; however, the time to knee minimum, time
to ankle drop-off, time to TP maximum during
stance, and time to ankle minimum during swing all
occurred considerably later for the high speed (Table
2). These trends suggest that some timing shifts
may be occurring in association with changes in
kinetics, if they are present.
Finally, given that the knee is the effective “hip”
in quail, I was concerned that using hip height to
compute Froude number would give spurious values
because the effective limb height (from the knee) is
about two-thirds that of the limb height based on the
hip. Surprisingly, using knee height instead produced only slightly higher Froude numbers and did
not change inferences about the walk–run transition. This may be because the animals were so small.
The position of the actual point of limb rotation
should be used in such calculations, especially given
that the addition of a moving fourth segment (the
femur, and its bulky muscle masses) at higher
speeds would have serious consequences to the
limb’s moment of inertia because both the radius of
rotation and the limb mass would be increased.
Obviously, more kinematic and force data for
more species are needed to discern possible shifts in
function, kinetics, and limb compliance dynamics
that may be associated with size effects and energetic constraints on bird locomotion.
ACKNOWLEDGMENTS
I thank Dennis Hartzler at the Ohio State University, Department of Animal Science in Wooster,
Ohio, for supplying the quail used in the study and
Nelson Frey of Ohio University Animal Resources
for making their stay here a happy one. Jason Elias
and Terry Kaylor assisted in the filming experiments and data logging and analysis. Staci Kehl
digitized the kinematics and assisted in data analysis. I thank Audrone Biknevicius, Ron Heinrich,
Larry Witmer, and the other members of the Locolab
Group at Ohio University for providing valuable
comments on the manuscript. I am especially grateful to Bruce Jayne, Peter Wainwright, and Garr
Updegraff for letting me use sMTV. Special thanks
to Tim Creamer who produced the kinematic photo
(Fig. 2). This research was supported by Ohio University Research Challenge Grant RC 95-025, an
Ohio University College of Osteopathic Medicine
Summer Undergraduate Research Fellowship, an
Ohio University Honors Tutorial College Summer
Research Fellowship, and National Science Foundation Grant IBN 9727212 to the author and Audrone
Biknevicius.
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