Performance of guinea fowl Numida meleagris during jumping requires storage and release of elastic energy
Department of Biology, Northeastern University, 360 Huntington Avenue, Boston, MA, 02115, USA
* Author for correspondence (e-mail: r.marsh{at}neu.edu)
Accepted 27 June 2005
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Summary |
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Key words: jumping, elastic energy storage, guinea fowl, Numida meleagris, power output, work output, takeoff, locomotion, kinematics, force plate, muscle
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Introduction |
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Small animals specialized for jumping produce an enormous amount of power
to accomplish the task of jumping. For example, during vertical jumping the
0.25 kg primate Galago senegalensis, the lesser galago or bush baby,
produces a muscle-mass-specific power output in excess of 2400 W
kg1 (Hall-Craggs,
1965; Gunther et al.,
1991
; Aerts, 1998
).
Small frogs also deliver impressive amounts of power during jumping. Peplowski
and Marsh (1997
) investigated
jumping performance of the Cuban tree frog Osteopilus septentrionalis
and predicted a peak muscle-mass-specific power output of the hindlimb muscles
of over 1600 W kg1, a value exceeding the power available
from the muscles by sevenfold. These extraordinary performances are made
possible by power amplification mechanisms involving elastic energy storage
and release. These mechanisms allow the animal to temporally redistribute the
work done by the muscles and transiently produce power in excess of that which
is available from direct power output by the muscle fibers alone.
Birds have been used in a variety of studies of walking, running and
flight, but their jumping performance has received much less scrutiny. Heppner
and Anderson (1985) investigated takeoff in the common pigeon Columba
livia and concluded that leg thrust represented a considerable
contribution to forces generated during takeoff. Earls (2000) focused on the
kinematics and mechanics of ground takeoff in the European starling
Sturnis vulgaris and the common quail Coturnix coturnix. Her
study discussed the evolution of flight in birds and illustrated the key role
that jumping plays in takeoff. Using a combination of kinematic and
force-plate data, Earls demonstrated that both species of birds performed
primarily leg-driven takeoffs; starling leg muscles produce 91% of the total
vertical velocity at lift-off and quail leg muscles account for 88% of the
total vertical velocity and 100% of the horizontal velocity. Neither of these
studies examined whether the measured jumping performance required elastic
energy storage and release.
The goal of our study was to examine what mechanisms for enhancing jumping
performance are available in a bird specialized for running, the helmeted
guinea fowl Numida meleagris. We asked whether during jumping these
animals rely on the same power amplification mechanisms used by more
specialized vertebrate jumpers, such as frogs and some primates. Because the
legs of guinea fowl are primarily used during terrestrial locomotion
performance, trade-offs may exist in order to achieve adequate performance in
both running and jumping. Helmeted guinea fowl were chosen for this study
because of their convenient size and ability to be readily trained to jump.
Untrained birds were observed to spontaneously jump to heights of up to 1 m.
Additionally, their taxonomic relationship to the common quail facilitates
comparisons between our data and that obtained by Earls (2000). Guinea fowl
are native to West Africa and locomote primarily by running; they seldom fly
unless startled and attempting escape
(Ayeni, 1982
). We hypothesized
that the jumping performance of guinea fowl would be sufficient to require
prestorage of elastic energy to power maximal jumps.
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Materials and methods |
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Mass of leg muscles that could power the jump
At the end of the jumping trials, the animals were sacrificed with an
overdose of sodium pentobarbital. Within 24 h ofdeath, all the hindlimb
muscles were dissected and weighed. The individual masses were recorded and
the sum of the masses of all the muscles (Mm) calculated.
For the purposes of calculating muscle-mass-specific work and power we summed
the masses of all the muscles that could possibly have contributed to jumping
(Mm,j). We excluded six muscles from this sum because
these muscles are anatomically positioned so that they could not produce
moments leading to extension at the hip, knee or ankle, or flexion at the toe
joint (Hudson, 1959; Gatesy,
1999). These muscles were the iliotrochantericus medius and
cranialis, the tibialis cranialis, the extensor digitorum longus, the
iliotibialis cranialis and the anterior portion of the iliofibularis. The
iliotibialis cranialis, which is a swing phase muscle in running
(Marsh et al., 2004
), can
produce a knee extensor moment, but the hip flexor moment arm of this muscle
is much larger than the knee extensor moment arm. Given that during jumping
the amount of hip extension is larger than the amount of knee extension (see
Results), the iliotibialis cranialis probably cannot shorten and do positive
work in the jump. A similar argument applies to the anterior portion of the
iliofibularis, which is another swing phase muscle in running
(Marsh et al., 2004
). This
portion of the iliofibularis has a very small hip extensor moment arm and a
large flexor knee flexor moment arm (T. A. Hoogendyk, personal
communication).
Training
The goal of our study was to isolate, as much as possible, the jumping
performance powered by the leg muscles from contributions of the wings
occurring before toe-off. Therefore, we designed a task that involved a nearly
vertical jump, with no subsequent phase of powered flight. The jumping regimen
consisted of conditioning the birds to jump from a platform up and through the
open door of an otherwise enclosed cage. The platform was gradually lowered,
thus encouraging the birds to perform higher jumps to reach the cage. Upon
completion of each successful jump, the bird was given a food reward of live
crickets. This jumping routine was conducted three times per week. The birds'
wings were clipped to reduce their contribution to the jump. Because these
birds were also used in a study comparing the function of the lateral
gastrocnemius in jumping and running, they were also trained to run on a
treadmill. The treadmill training regimen for running consisted of having the
birds run on a motorized treadmill using the following routine: 5 min at 1.5 m
s1, 10 min at 2.0 m s1, 3 min at 0.5 m
s1, and 12 min at 2.5 m s1. This regimen
was done three times a week to allow the birds to become accustomed to running
steadily on the treadmill. The birds underwent training for jumping and
running for a period of 68 weeks prior to experimentation.
Jumping procedures
The jumping arena was surrounded by a three-sided clear acrylic box. The
lateral sides of the box were 122 cm high and 91 cm long. The side behind the
bird was 46 cm high and 66 cm wide. The cage into which the birds jumped was
constructed of wire mesh with dimensions of 56 cmx75 cmx49 cm
(widthxlengthxheight). The cage was placed on a cart positioned at
the open side of the box. The jumping platform was placed on the floor within
the acrylic box. The platform was constructed of 2.5 cm thick plywood
measuring 30 cm long and 20 cm wide. A 10 cmx10 cm opening along the
right side of the platform was made to accommodate a force plate, which was
flush with the platform surface. The wooden platform and force plate were
raised and lowered by the addition or removal of 5 cm thick cement slabs (46
cmx15 cm). Maximal jumping height attained was 84 cm from the platform
to the bottom of the open cage door into which the bird jumped.
The force plate consisted of an aluminum plate (10 cmx10 cm) bolted
to a single triaxial quartz force transducer (Model 9067, Kistler, Winterthur,
Switzerland) capable of measuring three orthogonal components of a dynamic or
quasistatic force. The transducer was pre-stressed between two steel plates.
There was low cross talk amongst the channels on the force transducer
(FzFx,Fy
±1%; Fx
Fy
3%;
Fx,Fy
Fz
3%) and resonance frequencies ranged from 400 Hz to 800 Hz, depending on
the direction of measurement. The transducer was connected to 3, Type 5010,
Kistler charge amplifiers. The outputs from the amplifiers were connected to a
16-bit multiplexed AD converter (PowerLab model 16 sp, ADInstruments,
Colorado Springs, CO, USA) interfaced with a Macintosh G4 computer running the
application chart from ADInstruments. Data were collected at 2000 Hz. Each
force component was calibrated by first zeroing the output and loading the
plate uniaxially with a known weight. Weights were chosen to be within the
normal range of forces measured in the jumps. Mediolateral forces are not
discussed here because, for jumps parallel to the sagittal plane of the
animal, the mediolateral force produced by one leg is cancelled by an equal
and opposite force produced by the contralateral leg.
Videography
For the measurements reported here, the platform was positioned
approximately 84 cm beneath the cage opening. The jumps were video taped from
a lateral view at 500 frames s1 using a high-speed video
system (NAC HSV1000, Simi Valley, CA, USA). Only jumps in which it
could be verified that only one foot was on the force platform were analyzed.
Verification was done by placing a digital video camera at the rear of the
jumping platform to give a clear view of foot placement throughout the jump.
Video measurements were synchronized to force measurements using a square-wave
signal generated by the PowerLab and recorded on the video fields using a NAC
wave inserter.
Birds were prepared for the measurements by trimming feathers where needed and placing a series of markers on the body (Fig. 1). One marker was placed on the back immediately above the hip joint; a second marker was placed at the midpoint between the base of the neck and synsacrum; a third marker was placed on the anterior end of the sternum. The centers of the hip, knee, ankle (tibiotarsaltarsometatarsal) and toe (tarsometatarsalphalangeal) joints were marked with white dots. The tip of digit III was also painted white.
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The hip, ankle and toe markers were tracked in every frame and used in the
joint angle calculations. The position of the knee joint cannot be determined
accurately throughout the jump using a surface marker because of movement of
the skin, particularly during the pre-jump crouch. However, using the law of
cosines, knee angle can be calculated from the distance between the hip and
ankle joint centers, assuming constant segment lengths of the femur and
tibiotarsus. Femoral and tibiotarsal segment lengths were estimated from
average lengths measured from five video fields during which the knee angle
was approximately 90°. At this angle, the knee joint marker accurately
reflects the joint center. Angles were reported such that extension of the
hip, knee and ankle joints and flexion of the toe joint cause an increase in
angle (Fig. 1). This convention
reflects the expectation that active extension of the hip, knee and ankle
joints, and active flexion of the toe joint will contribute to powering the
jump. The approximate center of mass was determined by averaging the positions
of the sternum and synsacrum markers (Earls, 2000). Tracking the center of
mass in this way does not correct for changes in the center of mass due to leg
extension (see Results and Discussion).
Kinematically determined performance variables were calculated by tracking
the position of the center of mass. Values determined from kinematics are
designated by the subscript ki. Vertical and horizontal position data for the
center of mass were smoothed using a smoothing spline interpolation in the
software application Igor Pro (Wavemetrics, Lake Oswego, OR, USA). Vertical
(VV,ki) and horizontal (VH,ki) velocities
in m s1 were obtained by differentiating the smoothed
displacement data and vertical (aV,ki) and horizontal
(aH,ki) accelerations were obtained by differentiation of
the velocity curves. Horizontal force (FH,ki) in N was
calculated as
FH,ki=MbaH,ki;
vertical force (FV,ki) in N was calculated as
FV,ki=MbaV,ki+gMb
(where Mb is body mass and g is
gravitational acceleration). Resultant takeoff velocity
(Vres,ki) was calculated as the vector sum of the vertical
and horizontal velocities:
.
Horizontal (
H,ki) and
vertical (
V,ki)
muscle-mass-specific powers were calculated as the product of force and
velocity divided by Mm,j:
H,ki=(FH,kiVH,ki)/Mm,j
and
V,ki=(FV,kiVV,ki)/Mm,j.
Total muscle-mass-specific power output
(
sum,ki) was calculated as
the sum of
H,ki and
V,ki. Muscle-mass-specific
work output (Wsum,ki) was calculated by integrating
sum,ki with respect to time
during toe-off. Toe-off angle (
) was calculated as the arctangent of the
slope of the Y coordinates vs the X coordinates at
toe-off.
Calculating muscle performance from ground reaction forces
Performance variables calculated from force-plate data are designated by
the subscript fp. Performance was also calculated based on horizontal
(FH,fp) and vertical (FV,fp) forces
measured using the force plate. The total forces acting on the ground were
assumed to be twice the measured single-leg forces. Horizontal
(aH,fp) and vertical (aV,fp) accelerations
were calculated as:
aH,fp=FH,fp/Mb and
aV,fp=(FV,fpgMb)/Mb.
Horizontal (VH,fp) and vertical (VV,fp)
velocities were calculated by integration of aH,fp and
aV,fp. Integration started at the point at which the center
of mass no longer moved downward as determined from the video analysis (Earls, 2000). Muscle-mass-specific vertical
(
V,fp) and horizontal
powers (
H,fp) were
calculated by
V,fp=(FV,fpVV,fp)/Mm,j
and
H,fp=(FH,fpVH,fp)/Mm,j.
Muscle-mass-specific total power
(
sum,fp) was determined by
summing these powers and total work (Wsum,fp) calculated
by integrating
sum,fp with
respect to time.
Statistics
The summary data are presented as means ±
S.E.M. The values reported are based on
estimates for each bird representing the mean of 24 jumps for a total
of 18 jumps. The mean and S.E.M. for jumps
presented in the text and Table
2 are based on N=18. The total N based on the
individual jumps was used because we wanted to compare the two methods used
for calculating performance. Paired t-tests were used to examine the
differences between data for the same jumps calculated from kinematics and
from force-plate data. In order to compare guinea fowl data with the data of
Earls (2000), the jumps from
each animal were averaged and means ±
S.E.M. calculated using N=6.
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Results |
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General description of the jump
The jump was preceded by a pre-jump crouching movement characterized by
joint flexion (Figs 2,
3). The duration of the
crouching movement was quite variable. The mean crouch duration was
400±69 ms (N=18). We defined the jump as beginning with the
start of upward movement of the center of mass and ending with the last
contact of the toes with the ground (toe-off). The jump duration was much
shorter than the crouch duration and was much less variable. The jump had a
mean duration of 130±3 ms (N=18). The wings remained close to
the body throughout the crouch. As the bird lowered itself during the crouch
the wings were lowered slightly. When the bird began the jump, the wings began
to move away from the body and upwards. The wings continued to extend as the
bird continued its upward movement and achieved maximum extension
approximately 20 ms prior to toe-off. The wings remained extended as the bird
continued to move upwards and they began a downstroke just prior to
toe-off.
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The pre-jump crouch did not appear to represent a rapid countermovement designed to enhance jumping performance. In a countermovement jump, the potential energy of the body is first converted to kinetic energy, which may be stored as elastic strain energy as the body decelerates at the end of the countermovement. In the guinea fowl jumps, the body was lowered slowly (mean maximum downward vertical velocity=0.388 m s1), and the maximum kinetic energy in the downward movement represents only 0.40 J kg1 of leg muscle, or approximately 1% of the work produced in the subsequent jump phase (see Jumping performance).
Joint angles
Joint angles followed a characteristic sequence during jumping
(Fig. 3). The timing of the
minimum angles reached after crouching was calculated relative to the start of
the jump, defined as the time when the vertical accelerations became positive.
The hip started with a mean angle of 43.8±5° during standing and
gradually flexed throughout the crouch reaching a minimum angle of
30.3±9° at 20±18 ms. From this point the joint
gradually extended to a mean of 98±3° at toe-off. The knee joint
began at an angle of 64.8±3° and flexed slightly during the crouch,
reaching a minimum angle of 54.3±4° occurring at
36±43 ms. The knee reached maximum extension at lift-off at a
mean angle 97±4°. The ankle started the crouch at an angle of
90±10° and flexed to a minimum angle of 45±5° at
20±12 ms. The ankle joint had the largest angular change during the
jump, reaching a maximum of 154±5° at toe-off. The angle measured
at the toe joint results in an increase in angle for anatomically defined
flexion (see Materials and methods). The toe joint began at an angle of
132±8° and gradually flexed throughout the pre-jump crouch. At the
start of the jump, the toe joint begins a rapid extension reaching a minimum
of 115±2°. Late in the jump the toe started to flex rapidly and
reached a maximum angle of 173±4.77° just after toe-off. In
general, the beginning of hip extension occurred first or approximately at the
same time as the start of knee extension, ankle extension occurred somewhat
later and toe flexion occurred last.
Jumping performance
The center of mass of the bird is lowered by 0.09±0.04 m during the
pre-jump crouch and subsequently moves upward by 0.25±0.02 m before
toe-off (Fig. 4). Maximum
vertical and horizontal velocities were achieved just prior to toe-off
(Fig. 5). The vertical and
horizontal velocities at toe-off were approximately 3.3 m s1
and 1.3 m s1, respectively yielding a resultant velocity of
3.6 m s1 (Table
2). The peak velocities measured from kinematics and calculated
from the force-plate data were not significantly different
(Table 2). However, the rise in
the velocity of the bird's center of mass as measured from the kinematics
(using a constant point on the body of the bird) preceded the velocity
calculated from the force-plate measurements
(Fig. 5).
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Muscle-mass-specific power output peaked just prior to toe-off (Fig. 7). The values for peak horizontal power (76.09±8.74 W kg1 and 71.98±8.08 W kg1) calculated by the two methods were similar (Table 2). However, the mean of the peak vertical power calculated from the force-plate data (701.56±29.20 W kg1) was significantly greater (P=0.018) than the peak value calculated from kinematics (640.31±16.79 W kg1). Because of this difference, the total muscle-mass-specific peak power was also significantly higher (P=0.016) when calculated from the force-plate data (777.64±32.97 W kg1) than when the kinematic data were used (712.29±19.38 W kg1) (Fig. 8). The values of muscle-mass-specific power averaged over the entire jump (330 W kg1) were identical for the two methods and, thus, so was the muscle-mass specific work output (45 J kg1).
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Discussion |
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We attempted to design our experiments to exclude any contribution of the
flight muscles to the velocity attained at toe-off. We kept the primary and
secondary feathers of the birds clipped and trained the birds to jump from a
platform to a cage rather than performing a jump followed by a flight.
However, the birds did at times flap their wings following the jump.
Therefore, we followed Earls
(2000) and calculated
performance from both kinematic data and force-plate records. Earls
(2000
) found that in the common
quail, the first downstroke of the wings preceded the time at which the toes
left the ground. Therefore, the actual toe-off velocity she measured from
kinematics was higher than the value she calculated from force-plate data
(Table 3). Based on the
resultant toe-off velocities reported by Earls
(2000
), the wings contributed
18% of the kinetic energy present at takeoff.
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In contrast to the common quail, the first downstroke of the wings by the guinea fowl in our experiments began almost coincident with or slightly after toe-off. Consequently, the measured velocity of the center of mass at toe-off based on kinematics was the same as that calculated from the ground reaction forces (Table 2). Therefore, the leg muscles provided all the work required to lift the body weight against gravity and accelerate the bird's mass before toe-off. (These results may have been different if we had examined jumps that preceded a flight.)
Although the work and average power calculated by the two methods were
identical (Table 2), the peak
power calculated from the force-plate data was significantly higher than the
value calculated from the kinematics data
(Table 2,
Fig. 8). This difference likely
results from two factors that both tend to reduce the power calculated from
kinematics. First, the smoothing of the position data that was required before
the differentiation steps could have resulted in an underestimate of peak
power. Second, a consistent temporal offset was observed between force
measured from the force plate and that calculated from kinematics. This offset
could be due to the method used to estimate the center of mass in the
kinematic analysis. In this method, it was assumed that the center of mass was
a fixed point on the bird's body throughout the jump
(Earls, 2000). The true center
of mass is determined by the distribution of the masses of all the body
segments and this distribution changes throughout the jump. Leg extension
causes the center of mass to move downward and backward relative to the body.
The results of this movement of the center of mass, which was not considered
in our kinematic analyses, would have been be an overestimate of the early
acceleration of the center of mass and an underestimate of the acceleration
later in the jump. Essentially, the leg segments were initially moving slower
than the body but must have caught up late in the jump because the velocities
of all segments are equal at takeoff. The fact that the measured peak forces
and the power outputs calculated from force-plate data occurred later in the
jump than the values calculated from kinematics is consistent with this type
of error.
The toe-off velocity of guinea fowl measured by us and the value of Earls
(2000) for the common quail
(3.6 and 3.9 m s1, respectively) are consistent with the
hypothesis that most or all of the acceleration required for the rapid, steep,
escape flights of phasianids is achieved before the birds leave the ground and
involves very high work and power outputs by the leg muscles. Horizontal and
vertical flight velocities shortly after takeoff have been reported for five
species of phasianids (Askew et al.,
2001
). The resultant flight velocities for these species are all
less than 3.3 m s1 except for the value of 4.9 m
s1 reported for the very small (44 g) blue-breasted quail.
The powers required from the flight muscles of these birds are very high just
to maintain upward velocities after takeoff
(Askew et al., 2001
). Thus,
attaining the high rates of vertical acceleration seen in the jump would
probably not be possible using the flight muscles alone.
Power amplification by elastic storage and release
How does the level of muscle performance by guinea fowl leg muscles compare
with the direct power and work outputs expected from these muscles? To provide
a conservative estimate of performance, we assumed that the jumps were powered
equally by all the leg muscles capable of producing positive power, based on
their anatomically inferred actions (see Materials and methods). Peplowski and
Marsh (1997) calculated that
vertebrate skeletal muscles used in jumping are likely limited to
approximately 6070 J kg1 of work in a single rapid
contraction, as occurs during jumping. Guinea fowl, despite their apparent
lack of specialization for jumping, produce muscle work outputs of 45 J
kg1, or approximately 2/3 of the maximal expected value.
Although work outputs are expected to be similar among different muscles with
similar maximal forces and excursions, the maximal isotonic power expected
from a muscle will vary with its maximal shortening velocity and the curvature
of the forcevelocity relation. Isotonic power outputs are not known for
guinea fowl, but Nelson et al.
(2004
) report values of
approximately 320 and 340 W kg1 for two of the large lower
leg muscles of turkeys. Adjusting for the expected higher shortening velocity
of the smaller guinea fowl gives an estimate of approximately 380 W
kg1 for guinea fowl leg muscles. The average power of
approximately 330 W kg1 produced by the leg muscles in
jumping is within this estimate of the maximum direct power output. However,
to satisfy the peak power outputs measured during the jump, the muscles would
have to deliver approximately 800 W kg1, which is clearly
beyond their capacities. Elastic energy storage early in the jump and its
release during peak power production provides the mechanism to account for the
high peak power (Marsh and John-Alder,
1994
; Roberts and Marsh,
2003
).
The fact that the average power is within the limits of the muscles
suggests that the mechanism of the jump may not require much pre-storage of
elastic energy before the center of mass starts to move, as is the case in
some small jumpers (Bennet-Clark,
1975; Peplowski and Marsh,
1997
). Elastic energy storage and release within the jump suggests
the operation of an inertial catch mechanism, as described by Roberts and
Marsh (2003
). In this
mechanism an initially poor mechanical advantage in terms of producing ground
reaction force, allows muscles to initially shorten and stretch elastic
elements, presumably tendons. An improving mechanical advantage later in the
jump produces further rapid shortening and also release of the stored elastic
energy.
The values we report for the maximal power, nearly 800 W kg1, and work, approximately 45 J kg1, from the leg muscles as a group are likely to be underestimates of the performance of some of the individual muscletendon units. All the muscles identified as possibly participating in jumping are unlikely to have contributed equally to the work and power outputs. For example, the parallel-fibered hip and knee extensors that lack significant tendons may not be able to pre-store elastic energy as well as the pinnate muscles with long tendons.
Comparison with more specialized jumpers
How does the jumping performance of guinea fowl compare to that of more
specialized jumpers? Some small vertebrate jumpers have truly impressive
jumping performances that require substantial storage and release of elastic
strain energy. For example, Peplowski and Marsh
(1997) estimated that Cuban
tree frogs with an average body mass of 13 g produce a peak power exceeding
1600 W kg1 of muscle, about 7 times that available from
direct muscle power output. Because even the average power output (>800 W
kg1) of these small frogs during the jump exceeds the
expected muscle power output by a considerable margin, the jumping mechanism
likely involves an anatomical catch. An anatomical catch would allow
pre-storage of elastic energy before the jump begins, as has been found in
insects (Bennet-Clark, 1975
).
The presence of a substantial period of muscle activity before Cuban tree
frogs begin to accelerate has been confirmed with EMG recordings (R. L. Marsh
and M. M. Peplowski, unpublished observations). Predicted work outputs for the
muscles of these frogs (
60 J kg1) are high but within
the expected limits for vertebrate muscle. Among mammals, some primates are
particularly specialized for jumping. Bush babies Galago
senegalensis, which weigh about 250 g, perform jumps requiring a peak
power output of more than 2400 W kg1 of muscle
(Halls-Craggs, 1965; Gunther et al.,
1991
; Aerts, 1998
).
Work outputs of these animals probably approach the value of 70 J
kg1 suggested as the maximum possible. (These values for
power and work depend on assumptions about which muscles are involved in the
jump. Muscle masses are given in Grande,
1977
). Despite their greater muscle-mass-specific work and power,
these primates may be similar to guinea fowl in not pre-storing a lot of
energy before the start of the jump. Based the detailed force-plate records
published by Gunther et al.
(1991
), the Galago
has a substantial period of slow acceleration at the beginning of the jump.
Calculations from these records indicate that, although the peak power output
of the muscles exceeds 2400 W kg1, the average power output
may be approximately 450 W kg1. The properties of
Galago muscles are not known, but very fast lizard muscles can
generate an isotonic power of 460 W kg1 at 40°C
(Marsh and Bennett, 1985
).
The approximately 800 W kg1 of muscle-mass-specific peak
power found here during guinea fowl jumping is clearly lower than the values
found for these specialized jumpers. However, producing muscle-mass-specific
work outputs of 45 J kg1 is a surprisingly good performance
for these non-specialized jumpers. Also, in judging the peak power outputs,
the larger body size (approximately 1.5 kg) of the guinea fowl relative to the
Cuban tree frog and Galago should be taken into consideration.
Generally, elastic storage mechanisms are expected to be more important for
small animals (Bennet-Clark,
1977; Alexander,
1995
). This size effect is seen clearly in the two species of
phasianid birds that have been studied. The common quail studied by Earls
(2000
) achieves a similar
leg-powered toe-off velocity, and thus a similar body-mass-specific work
output, as that of the guinea fowl, but reaches this velocity in about 2/3 of
the time. If these species have similar fractions of their body mass devoted
to leg muscles, the expected muscle power outputs of the quail leg muscles
would be 1.5 times those of the guinea fowl muscles.
Conclusion
This study has demonstrated that during jumping guinea fowl produce power
in excess of the power directly available from their leg muscles. We conclude
that elastic storage and recovery of energy in tendons likely provides the
mechanism for temporally redistributing the work done by the muscles during
jumping. Likely sites for the storage of elastic energy include the tendons of
the ankle extensors.
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Acknowledgments |
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References |
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Aerts, P. (1998). Vertical jumping in Galago senegalensis: the quest for an obligate mechanical power amplifier. Phil. Trans. R. Soc. Lond. B 353,1607 -1620.[CrossRef]
Alexander, R. McN. (1995). Leg design and jumping technique for humans, other vertebrates and insects. Phil. Trans. R. Soc. Lond. B 347,235 -248.[Medline]
Askew, G. N. and Marsh, R. L. (2001). The
mechanical power output of the pectoralis muscle of blue-breasted quail
(Coturnix chinensis): the in vivo length cycle and its
implications for muscle performance. J. Exp. Biol.
204,3587
-3600.
Askew, G. N., Marsh, R. L. and Ellington, C. P.
(2001). The mechanical power output of the flight muscles of
blue-breasted quail (Coturnix chinensis) during takeoff.
J. Exp. Biol. 204,3601
-3619.
Ayeni, J. S. O. (1982). Home range size, breeding behavior, and activities of helmeted guineafowl Numida meleagris in Nigeria. J. West. African. Ornithol. Soc. 5,37 -43.
Bennet-Clark, H. C. (1975). The energetics of the jump of the locust Schistocera gregaria. J. Exp. Biol. 63,53 -83.[Abstract]
Bennet-Clark, H. C. (1977). Scale effects in jumping animals. In Scale Effects in Animal Locomotion (ed. T. J. Pedley), pp. 185-201. New York: Academic Press.
Earls, K. (2000). Kinematics and mechanics of
ground takeoff in the starling Sturnis vulgaris and the quail
Coturnix coturnix. J. Exp. Biol..
203,725
-739.
Gatesy, S. M. (1999). Guineafowl hind limb function. II: Electromyographic analysis and motor pattern evolution. J. Morphol. 240,127 -142.[CrossRef]
Grande, T. I. (1977). Body weight: Its relations to tissue composition, segment distribution, and motor function. 1. Interspecific comparisons. Am. J. Phys. Anthropol. 47,211 -240.[Medline]
Gunther, M. M., Ishida, H., Kumakura, H. and Nakano, Y. (1991). The jump as a fast mode of locomotion in arboreal and terrestrial biotopes. Z. Morph. Anthropol. 78,341 -372.
Hall-Craggs, E. C. B. (1965). An analysis of the jump of the Lesser Galago (Galago senegalensis). J. Zool. 147,20 -29.
Heppner, F. H. and Anderson, J. G. T. (1984). Leg thrust in flight takeoff in the pigeon. J. Exp. Biol. 114,285 -288.
Hudson, G. E., Lanzillotti, P. J. and Edwards, G. D. (1959). Muscles of the pelvic limb in galliform birds. Am. Midl. Nat. 61,1 -67.
Marsh, R. L. and Bennett, A. F. (1985). Thermal dependence of isotonic contractile properties of skeletal muscle and sprint performance of the lizard Dipsosaurus dorsalis. J. Comp. Physiol. 155,541 -551.
Marsh, R. L. and John-Alder, H. B. (1994).
Jumping performance of hylid frogs measured with high-speed cine film.
J. Exp. Biol. 188,131
-141.
Marsh, R. L., Ellerby, D. J., Carr, J. A., Henry, H. T. and
Buchanan, C. I. (2004). Partitioning the energetics of
walking and running: Swinging the limbs is expensive.
Science 303,80
-83.
Nelson, F. E., Gabaldon, A. M. and Roberts, T. J. (2004). Force-velocity properties of two avian hindlimb muscles. Comp. Biochem. Physiol. 137A,711 -721.
Peplowski, M. M. and Marsh, R. L. (1997). Work
and power output in the hindlimb muscles of Cuban tree frogs Osteopilus
septentrionalis during jumping. J. Exp. Biol.
200,2861
-2870.
Rayner, J. M. (1979). A new approach to animal flight mechanics. J. Exp. Biol. 80, 17-54.
Roberts, T. J. and Marsh, R. L. (2003). Probing
the limits to muscle-powered accelerations: lessons from jumping bullfrogs.
J. Exp. Biol. 206,2567
-2580.
Tobalske, B. W. and Dial, K. P. (2000). Effects
of body size on takeoff flight performance in the Phasianidae (Aves).
J. Exp. Biol. 203,3319
-3332.
Witter, M. S., Cuthill, I. C. and Bosner, R. H. (1994). Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Anim. Behav. 48,201 -222.[CrossRef]
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