In vivo muscle activity in the hindlimb of the arboreal lizard, Chamaeleo calyptratus: general patterns and the effects of incline
Department of Biological Sciences, University of Cincinnati, PO Box 210006, Cincinnati, OH 45221-0006, USA
* Corresponding author at present address: Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA (e-mail: tehigham{at}ucdavis.edu)
Accepted 6 October 2003
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Summary |
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Key words: locomotion, lizard, C. calyptratus, arboreal, kinematics, incline, slope, hindlimb, electromyography, muscle
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Introduction |
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When an animal moves uphill, the opposing forces exerted by gravity
increase the cost of transport (Farley and
Emshwiller, 1996; Wickler et
al., 2000
) and the mechanical power required by propulsive-phase
muscles (Farley, 1997
;
Roberts et al., 1997
;
Swanson and Caldwell, 2000
;
Gabaldon et al., 2001
). In
contrast, during downhill locomotion increased activity of some muscles may be
required to slow the animal and retard passive flexion of the joints rather
than enhance the speed of forward movement and actively flex the joints
(Smith et al., 1998
;
Gabaldon et al., 2001
). Whether
motor patterns are altered similarly on inclines between animals that inhabit
structurally different habitats or between animals from evolutionarily diverse
lineages is not fully understood.
A key question in functional morphology is whether muscle activity is
conserved during major evolutionary changes in morphology and environment
(Peters and Goslow, 1983;
Lauder and Shaffer, 1988
;
Wainwright et al., 1989
;
Lauder, 1994
;
Smith, 1994
;
Ashley-Ross, 1995
;
Biewener, 2002
). Many animals
living in arboreal habitats have morphological, behavioral or ecological
specializations that allow them to move effectively in this habitat. For
example, primates and chameleons have prehensile feet
(Fig. 1;
Cartmill, 1974
;
Peterson, 1984
;
Schmitt, 1998
) and geckoes and
anoles have toe pads (Irschick et al.,
1996
; Russell,
2002
), all of which facilitate grasping perches in arboreal
habitats. Morphological specializations for arboreal habitats or the structure
of the habitat itself could result in the alteration of the ancestral motor
pattern of limb muscles during locomotion.
|
Lizard taxa vary considerably in their morphology, ecology and behavior,
and include both terrestrial and arboreal forms. Furthermore, many lizards are
adept at moving on steep inclines in their natural habitats. Inclines often
affect the maximal speeds (performance) and limb movements (kinematics) of
lizards in both laboratory and field experiments
(Huey and Hertz, 1982;
Irschick and Jayne, 1998
,
1999a
;
Jayne and Ellis, 1998
;
Jayne and Irschick, 1999
;
Zaaf et al., 2001
). However,
previous EMG experiments with lizards have neither examined the effects of
incline nor studied an arboreal species
(Jayne et al., 1990a
;
Reilly, 1995
;
Nelson and Jayne, 2001
). Thus,
we examined the effects of incline on the in vivo activity of
hindlimb muscles in the arboreal specialist C. calyptratus (veiled
chameleon) and correlated muscle activity to the three-dimensional movements
of the hindlimb.
Recording the limb movements and motor patterns of locomotion on different
inclines can provide fundamental insights into whether some biologically
realistic and important sources of environmental variation may require
fundamental changes in limb function or motor output. Thus, we addressed the
following major questions regarding the effects of incline on the muscle
activity in the hindlimb of C. calyptratus. (1) Are the muscle
activity patterns in the hindlimbs of chameleons affected by the incline of
the locomotor surface? We hypothesized that most muscle activity in chameleons
would be affected by incline as in other vertebrate taxa, such that the amount
of activity of propulsive muscles would be greatest on the uphill and least on
the downhill surface. Furthermore, the activity of muscles that prevent the
collapsing of joints would be greatest on the downhill surface. Based on a
study of chameleon kinematics (Higham and
Jayne, 2004), we hypothesized that chameleons would rely more on
actively pulling themselves forward on level and uphill surfaces. Thus, the
muscles that flex the knee and retract the limb during the early part of
stance may have disproportionately more activity. (2) Are the patterns of
muscle activity in the hindlimbs of chameleons similar to those of terrestrial
generalized lizards, despite substantial morphological differences? Although
the kinematics of chameleons differ from those of generalized lizards
(Higham and Jayne, 2004
), we
test the null hypothesis that motor pattern is conserved.
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Materials and methods |
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We determined the gross anatomy of the limb musculature by performing
dissections of preserved specimens and using the work of Mivart
(1870) and Snyder
(1954
). Our terminology
follows that of Snyder (1954
).
Nine large muscles were well suited for percutaneously implanting EMG
electrodes, and Fig. 1
illustrates the gross anatomy of these muscles.
Experimental protocol
We used Halothane to anesthetize all animals before implanting EMG
electrodes. Animals recovered from anesthesia for approximately 2 h before the
experiments began. C. calyptratus moved along a 2.4 cm diameter
wooden dowel, covered with cloth adhesive tape, with inclines of -45°
(downhill), 0° (level), and 45° (uphill) after their body temperature
reached 29-31°C, which is within the range of the active body temperatures
that we observed in the laboratory for this species
(Higham and Jayne, 2004). Each
individual was tested within a single day and the order of inclines was
randomized to minimize confounding effects of time. Following each experiment,
the lizard was euthanized, and post-mortem dissections confirmed the
position of EMG electrodes.
We obtained simultaneous dorsal and lateral views of the chameleons moving
on the perch using a two-camera NAC HSV-500 (Tokyo, Japan) high-speed video
system operating at 250 images s-1. Video recordings were
synchronized with EMG recordings using a 100 Hz square-wave generator that
provided output to both the video system and the EMG tape recordings. To
provide fixed points of reference, we drew lines at 10 cm intervals along the
length of the surfaces. To facilitate digitizing the location of points on the
lizards, we painted landmarks on the pelvis, knee, ankle, metatarsal and toe
tip, as in Higham and Jayne
(2004). Prior to each trial,
we measured the body temperature of the chameleon using a thermocouple and a
Tegam (Geneva, OH, USA) model 871A digital thermometer. From the video
footage, we selected 3-4 strides per individual per incline that had similar
speeds and duty factors among and within individuals. The grand means ±
S.E.M. for the speeds and duty factors for all of the 44 strides
were 11.2±0.5 cm s-1 and 58.7±0.7%, respectively.
Similar duty factors commonly indicate equivalent gaits, and an analysis of
variance (ANOVA) confirmed that duty factors did not vary significantly with
incline (F=2.8, P=0.07, d.f.=2,32) or among individuals
(F=2.6, P=0.07, d.f.=3,32). All of the locomotion of C.
calyptratus was a relatively slow walk.
For the chameleons, we analyzed non-consecutive strides from different trials, and the stationary surfaces used to obtain locomotion required a large number of trials to obtain reasonably steady-speed locomotion of similar speeds. The strides selected for analysis were in the middle of a bout of locomotion with three or more strides that subjectively appeared to be of similar speed. Hence, we selected strides with little if any acceleration.
Electromyography
We used fine-wire bipolar electrodes to record the in vivo
activity of the muscle, and the general methods for constructing the
electrodes followed those of Jayne
(1988). We used 0.051 mm
diameter polycoated stainless-steel wire (California Fine Wire Co., USA) with
approximately 0.7 mm of insulation removed from the recording end. A ground
wire was also implanted in the epaxial musculature of the proximal portion of
the tail. We implanted each electrode through the skin using a 26-gauge
hypodermic needle with the wires inserted through the tip. Following
implantation, we used cyanoacrylate glue to attach electrode wires to the skin
of the lizard's tail and plastic model cement to glue the two wires of each
electrode together and all electrodes together into a single cable. The
lengths of the wires from the animals to the probes of the recorder were
approximately 2 m, which was sufficiently long to allow the lizards to move
freely. We implanted a total of nine EMG electrodes into nine muscles of the
right hindlimb (Fig. 1).
Electromyograms (EMGs) were amplified 5000x using Grass P511k series
amplifiers (West Warwick, RI, USA) with high- and low-bandpass filters of 100
Hz and 10 KHz, respectively, and a 60 Hz notch filter. The analog EMG signals
were recorded at 9.5cm s-1 using a TEAC XR-7000 FM data recorder
(Tokyo, Japan). We converted the analog signals to digital data using a
Keithley 500A (Cleveland, OH, USA) analog-to-digital converter with an
effective sampling rate of 8 kHz (Jayne et
al., 1990b). Digital EMGs were filtered using a high-pass
finite-impulse response filter to reduce the amplitude of the signal below 100
Hz to less than 10% of the original amplitude.
We used customized computer software (written by Garr Updegraff, San Clemente, CA, USA; garru{at}uci.edu) to subdivide each stride into bins for three separate analyses. First, we subdivided the stance and swing phase of each stride into fifteenths and tenths, respectively. This was done to facilitate pooling data from different strides so that the number of bins during stance divided by the total number of bins per stride equalled 60%, which approximated the average duty factor for all of the strides. Consequently, each bin often covered approximately 4% of the total stride, but the absolute duration of bins within a stride or among strides varied slightly as a result of strides with variation in duty factor or total duration. The average rectified amplitude (RA) of each bin (rectified integrated area divided by bin duration) for each muscle was then converted to relative amplitude by dividing by the maximum value ever observed within a bin for a given individual and muscle. These data were used to generate a profile of mean relative amplitude pooled across all individuals for each incline with a 60% duty factor (the approximate mean value). Second, we subdivided each stride into 25 equal duration bins. The total rectified integrated area (RIA) for a given muscle was calculated per stride and the RIA for each bin was converted to relative area based on its percentage of the total RIA for the stride. For pairs of muscles within each stride we calculated the product moment correlation coefficients (r) between pairs of values of percent activity per bin per stride, using values from bins with the same elapsed time. We used these cross-correlations to clarify the extent to which the activity of different muscles overlapped. We expected synergistic and antagonistic pairs of muscles to have positive and negative correlations, respectively. Lastly, we subdivided each stride into 30 ms bins. We chose 30 ms (see Kinematics, below) so that at least one bin was available between successive video images that were digitized. We then summed the activity of all bins during a kinematic event and divided by the total per stride. Thus, for each muscle we could determine the percentage of activity that was during stance versus swing, joint extension versus flexion, etc.
For many muscles during downhill locomotion, large time intervals (>0.1 s) often elapsed between successive spikes of EMGs (e.g. Fig. 2, caudofemoralis, -45°), or the amplitudes of EMG spikes were often small. Thus, determining the onset and offset of EMGs for all experimental conditions was often not practical.
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From all four individuals in our study, we obtained EMGs from one hip muscle, the caudofemoralis (CF), four thigh muscles including the iliofibularis (IF), iliotibialis (IT), flexor tibialis externus (FTE) and puboischiotibialis (PIT), and four lower leg muscles including the gastrocnemius (G), tibialis anterior (TA), extensor digitorum longus (EDL) and the peroneus (P) (Fig. 1).
Kinematics
We used customized video analysis software (Measurement TV, written by Garr
Updergraff) to reconstruct the three-dimensional coordinates of each landmark.
The x-axis of each video image was parallel to the overall direction
of travel along the long axis of the locomotor surface. The y-axis
was perpendicular to the surface and within a vertical plane passing through
the long axis of each walkway, and y=0 for the top of the walkway
along its entire length. The z-axis was perpendicular to the
x-y plane.
For each chameleon on each incline, we digitized 27-32 images per stride, which provided images 30-150 ms apart. Three-dimensional coordinates were digitized for the right hip, knee, ankle, base and tip of the fourth toe (excluding claw). From a dorsal perspective, two-dimensional coordinates (x, z) were digitized for the right and left hips.
Three-dimensional angles described angles of joints within the hindlimb at
footfall and at the end of stance. A detailed explanation of the angular
measurements can be found in Jayne and Irschick
(1999). Smaller values of knee
angle between 0° and 180° indicate greater flexion of the joint. For
the ankle angle, decreasing values between 0° and 180° indicate
greater dorsiflexion of the foot. The orientation of the pelvis was determined
by a two-dimensional angle obtained from a dorsal (x, z) perspective,
and the amount of pelvic rotation equalled the differences between maximum and
minimum values.
For three angles that describe the orientation of the femur, we determined the maximum and minimum values for each complete stride cycle. Femur retraction was the two-dimensional angle between a line connecting the left and right hips and the long axis of the femur projected onto the x-z (horizontal) plane. Femur retraction values of 0° indicate when the femur is perpendicular to the longitudinal axis of the pelvis, and positive and negative values indicate measurements of femur retraction and protraction, respectively. Long-axis rotation of the femur was a three-dimensional angle between a vertical reference plane passing through the femur and the plane containing the femur and tibia. Greater clockwise long-axis rotation of the right femur, as seen in right lateral view, is indicated by greater positive values, and a value of zero indicates that the plane containing the femur and tibia is within the vertical reference plane passing through the femur. Femur depression was the three-dimensional angle between the long axis of the femur and a horizontal reference plane. Positive and negative values of femur depression indicate that the distal femur was either ventral or dorsal to the hip, respectively.
Statistical analyses
We used SAS version 8.0 for all statistical analyses, and
P<0.05 was the criterion for statistical significance. In the
tabular summaries of the statistics, we provide degrees of freedom and
F-values to clarify the potential effects of making multiple
comparisons. To analyze the extent to which muscle activity overlapped with
other muscles, we constructed correlation matrices and used the resulting
r-values in two-way analyses of variance (ANOVAs) with individual as
a random crossed factor and incline as a fixed crossed factor. The denominator
for the F-test on the incline effect was the two-way interaction
terms of the fixed effect and the individual factor
(Zar, 1996). To determine the
effects of incline on the angular variables, we performed ANOVAs on each
angular variable with incline and individual as the independent variables.
Finally, to determine whether incline significantly affected the percentage of
activity of a certain muscle during a particular kinematic event, we performed
ANOVAs on each percentage with incline and individual as the independent
variables.
Results are presented as means ± S.E.M., unless stated otherwise.
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Results |
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The gastrocnemius (G) originates from both the distal part of the femur and the posterior aspect of the tibia and runs along the posterior edge of the lower leg where it inserts on the plantar ossicle (Fig. 1D). The extensor digitorum longus (EDL) originates from the distal portion of the femur and from the posterior portion of the fibula and inserts onto both the fourth and fifth digit (Fig. 1C,D). The peroneus (P) originates from the proximal portion of the anterior face of the fibula and from the proximal portion of the posterior tibia and inserts on the proximal and dorsal portion of the fifth metatarsal (Fig. 1B). The tibialis anterior (TA) originates from the proximal portion of the tibia and inserts onto the proximal portion of the first metatarsal (Fig. 1C,D). Table 1 summarizes the hypothesized actions of the muscles based on their gross anatomy.
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General description of limb movements and the effects of incline
At footfall, the knee of C. calyptratus extended well beyond
90° and the femur was protracted (Fig.
2A), which positioned the foot anterior to the hip. The angles of
both the knee and ankle at footfall usually exceeded 120° and 140°,
respectively (Fig. 2A). Maximal
pelvic rotation was approximately coincident with footfall. Femur retraction
of C. calyptratus began slowly at footfall, was fairly rapid at
midstance, and continued to a maximum slightly before the end of stance
(Fig. 2A). After footfall, the
knee flexed maximally to an acute angle near midstance, whereupon the knee
extended to a maximum at the end of stance
(Fig. 2A). Clockwise long-axis
femur rotation (as seen in right lateral view) began at footfall and continued
throughout stance (Fig. 2A). Femur depression remained fairly constant throughout stance
(Fig. 2A).
At the beginning of swing, the knee began to flex until just before mid-swing and then extended until footfall (Fig. 2A). The amount of knee flexion during swing was always less than the amount of flexion during stance. Femur protraction began at the beginning of swing and was rapid until mid-swing, whereupon the femur was protracted slowly until footfall (Fig. 2A). Counterclockwise long-axis femur rotation of C. calyptratus also began near the beginning of swing, was rapid until mid-swing, and continued rotating slowly until footfall (Fig. 2A). Values of femur depression decreased sufficiently during early swing such that the knee was often more dorsal than the hip. From mid-swing until footfall, femur depression remained relatively constant (Fig. 2A).
Incline significantly affected only one of the 19 angular variables
measured, which is similar to the minimal effect of incline on kinematics of
C. calyptratus found by Higham and Jayne
(2004). The ankle angle at the
end of stance was significantly affected by incline such that the greatest
values were on the downhill and lowest on uphill surface
(Fig. 2A). The speeds of
locomotion for the kinematic data in Higham and Jayne
(2004
) and this study were
very slow (grand means=17 and 11 cm s-1, respectively) and the duty
factors were similar (grand means=63% and 59%, respectively). Thus, we had no
evidence that the electrodes substantially affected the locomotion of the
chameleons in this study compared to the previous kinematic study.
Muscle activity on a level perch
The average duty factor was approximately 60%, thus a muscle with constant
amplitude and continuous activity would have 60% activity during stance and
40% during swing. More than two-thirds of the rectified integrated area (RIA)
occurred during stance for the caudofemoralis, flexor tibialis externus,
puboischiotibialis, extensor digitorum longus, and peroneus regardless of
incline (Table 2).
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The onset of caudofemoralis activity began immediately following footfall and usually continued throughout the stance phase of the stride (Fig. 2B). The activity of the caudofemoralis usually ceased just after the beginning of the swing phase (Fig. 2B). The location of burst activity of the iliofibularis during a stride varied considerably between individuals. Occasionally a small burst of iliofibularis activity occurred during early stance, but most commonly the burst of iliofibularis activity was at the beginning of swing (Fig. 2B). The iliotibialis usually had one burst of activity beginning at midstance and continuing until the end of stance and another burst near mid-swing (Fig. 2B). The activity of the flexor tibialis externus began immediately following footfall and usually ended near midstance (Fig. 2B). The puboischiotibialis had an initial burst of activity immediately following footfall and lasting for approximately one-fourth of stance, and a second burst of activity occurred at the beginning of swing and lasted for approximately one-fourth of the swing phase (Fig. 2B).
The gastrocnemius was active throughout stance and had lower amounts of activity throughout swing (Fig. 2B). The tibialis anterior had variable activity that often occurred throughout the stride (Fig. 2B). The extensor digitorum longus had a strong burst of activity immediately following footfall and lasted for up to one-half of stance (Fig. 2B). A second burst of activity of the extensor digitorum longus with lower amplitude and relatively short duration occurred just before mid-swing (Fig. 2B). The peroneus became active at footfall or just prior to the end of swing and was active for approximately half of stance (Fig. 2B).
The only significant negative cross-correlation of relative EMG amplitude between pairs of muscles for locomotion on the level perch was for the iliotibialis and the puboischiotibialis (Table 3), and the near absence of overlapping activity of these two muscles (Figs 2, 3) agrees well with their antagonistic functions as a knee extensor and flexor, respectively. Several of the lower limb muscles had substantial overlap of major activity (Figs 2, 3), and hence significant positive cross correlations between the relative amplitudes of activity (Table 3).
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Effects of incline on muscle activity
The effects of incline were more conspicuous for hip and thigh muscles than
for lower leg muscles (Figs 2,
3). Furthermore, changes in
motor pattern in response to incline were predominantly due to changes in
amplitude rather than changes in timing (Figs
2,
3). Effectively all of the
muscles studied had less intense activity for downhill locomotion than for
both level and uphill locomotion.
The percentage of muscle activity during stance changed significantly with incline for the caudofemoralis, which had much more of its activity during stance on level (93%) and uphill (86%) than on the downhill (67%) (Table 2). The peak relative amplitude of the caudofemoralis within an entire stride increased from downhill to level and from level to uphill (Fig. 3). Large amplitude activity of the caudofemoralis was conspicuously absent during early stance as the knee flexed on the downhill compared to the level and uphill surfaces (Fig. 3; Table 2). Effectively no caudofemoralis activity occurred in early swing as the knee flexed during level and uphill locomotion, whereas a significantly greater amount of activity occurred during this time interval for downhill strides (Fig. 3; Table 2).
Activity of the iliotibialis was nearly absent during early stance on the level and uphill surfaces, and the peak relative amplitude per stride increased from downhill to level and level to uphill (Fig. 3). On the uphill surface, more than half the iliotibialis activity occurred as the knee extended during stance and there was significantly less activity during this period for strides on the level and downhill surfaces (Table 2).
The peak activity of the flexor tibialis externus during the entire stride on the downhill surface was markedly less than the values for both the level and uphill surfaces (Fig. 3). Additionally, the amount of flexor tibialis activity during knee flexion during stance on the downhill was less that half that of the uphill and level surfaces (Table 2).
The peak activity per stride of the puboischiotibialis increased from downhill to level and from level to uphill (Fig. 3). For the puboischiotibialis a clear maximum in relative amplitude occurred shortly after footfall on the uphill and level surfaces (Fig. 3), and the percentage of activity during knee flexion within stance for uphill and level strides was approximately twice that of downhill strides (Table 2).
Most cross-correlations of muscle activity were not affected greatly by incline (Table 3). Only three of the 36 combinations of muscles were affected significantly by incline and each of these three pairs had higher cross correlations going from downhill to level and from level to uphill (Table 3). Although the cross correlations between activity of the iliotibialis and flexor tibialis externus muscles were not significantly affected by incline as indicated in the ANOVA, this negative cross correlation was significant for the level surface but not for either the downhill or uphill data. Thus, the overlap in activity of these two muscles was least on the level surface. The highly significant positive cross correlations for the level and uphill surfaces emphasize the similarity of the timing of peak activity of the flexor tibialis externus and the puboischiotibialis muscles near the beginning of stance, whereas the absence of a significant cross correlation for surface suggests these muscle do not retain fundamentally similar timing relationships on the downhill compared to the other surfaces.
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Discussion |
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At footfall, the femur of C. calyptratus is maximally protracted,
and unlike most lizards, the knee of C. calyptratus is extended well
beyond 90° (Higham and Jayne,
2004). Thus, knee flexion during early stance seems likely to pull
the body forward. Consequently, muscles that flex the knee during early stance
are likely to be important for propelling the body forward in a fashion
analogous to the salamander, Dicamptodon tenebrosus
(Ashley-Ross, 1995
). The
muscles most likely to be responsible for knee flexion during the first half
of stance in C. calyptratus are the flexor tibialis externus,
puboischiotibialis and the caudofemoralis. These muscles all had bursts of
activity during early stance and were all hypothesized to flex the knee, and
the greatest amplitude occurred immediately following footfall. Thus, actively
pulling the body forward is partly determined by the activity of these three
muscles. During femur retraction, the caudofemoralis and flexor tibialis
externus were active and thus could contribute to another mechanism of
propulsion.
Plantar flexion and dorsiflexion could not be measured as easily in
chameleons as in other lizards (Irschick
and Jayne, 1999b; Jayne and
Irschick, 1999
). The highly specialized foot of C.
calyptratus has two opposing groups of digits, each of which is enclosed
in skin, rather than having five independent digits
(Fig. 1). We measured ankle
angle as the three-dimensional angle between the lower limb and the fourth
metatarsal (within the lateral group of digits). Consequently, the ankle angle
is affected both by closing and opening the foot (to grasp and release the
perch) and posteriorly directed movements of the collective foot structures
relative to the lower limb. The movements of the chameleon feet were also not
on a flat substrate as they grasped the round perch. Thus, we assumed that the
functional equivalent of plantar flexion occurred predominantly during stance
and the reverse movement occurred during swing. The anatomy of the peroneus
and gastrocnemius and the large portion of their activity during stance
suggest that these muscles are involved in the posterior rotation of the foot
in C. calyptratus.
The hyperextension of the toe at the end of stance and very early swing in
many terrestrial lizards (Irschick and
Jayne, 1999b; Jayne and
Irschick, 1999
) suggests that using the foot to actively push off
from the flat substrate is important. In contrast, the change of nearly
90° in the orientation of the long axis of the foot of C.
calyptratus largely precludes this mechanism of propulsion. Furthermore,
the foot of C. calyptratus grasps the perch and does not hyperextend
at the end of stance. The grasping foot of chameleons could thus facilitate a
mechanism for propulsion that relies on pulling the body, but at the cost of a
reduced ability to push during late stance by plantar flexion similar to that
of other terrestrial lizards.
Comparisons with alligators and lizards
The caudofemoralis of both crocodilians and lepidosaur reptiles is a robust
muscle originating from caudal vertebrae and inserting on the femur and
proximal lower limb and is involved in femur retraction, posterior femur
rotation and knee flexion (Gatesy,
1990,
1997
;
Russell and Bauer, 1992
;
Reilly, 1995
;
Nelson and Jayne, 2001
).
Previous EMG studies of lizards and crocodilians have found that the
caudofemoralis usually becomes active late in swing, which could retard femur
protraction, anterior femur rotation and knee extension
(Reilly, 1995
;
Gatesy, 1997
;
Nelson and Jayne, 2001
). The
onset of activity of the caudofemoralis of C. calyptratus was usually
at footfall and only rarely during late swing. However, the slow locomotor
speed of C. calyptratus may preclude the need to actively decelerate
femur protraction with the caudofemoralis.
Nelson and Jayne (2001)
found that passive changes in strain of the caudofemoralis muscle of the
desert iguana, Dipsosaurus dorsalis, were only affected by knee
extension when the femur was substantially anterior to the hip. Thus, although
the caudofemoralis of C. calyptratus appears likely to flex the knee
during early stance, the lack of activity and position of the femur suggest
the caudofemoralis is not important for the second flexion of the knee during
swing.
We found that the activity of the iliofibularis of C. calyptratus
was variable but when a burst was evident, it was usually in early swing
(Fig. 2). The activity of the
iliofibularis of Alligator mississippiensis starts during late stance
and continues into early swing (Gatesy,
1997), and the iliofibularis of the savannah monitor, Varanus
exanthematicus, is active mainly during swing
(Jayne et al., 1990a
).
The puboischiotibialis of alligators has two distinct bursts, one from late
swing to late stance, and another shorter burst at the stance/swing transition
(Gatesy, 1997). In alligators,
the puboischiotibialis probably helps to prevent limb collapse during stance
by resisting femoral abduction (Gatesy,
1997
). The activity of the pubotibialis (similar to our PIT) of
Sceloporus clarkii begins after footfall and peaks when the knee
angle is 90° (Reilly,
1995
), thus contributing to knee flexion. A smaller burst of
activity in S. clarki also occurs at mid-swing
(Reilly, 1995
). Similarly, the
puboischiotibialis of C. calyptratus had two very distinct bursts,
but one burst was in early to mid-swing and the other was in early stance.
Thus, the timing of activity of the puboischiotibialis of C.
calyptratus is different from that of the distantly related alligator,
but relatively similar to S. clarki. The burst of activity in early
stance could help maintain the horizontal orientation of the femur and thus
prevent femur elevation.
The gastrocnemius and peroneus longus of Sceloporus clarki are
both plantar flexors that have peak bursts during the first half of stance
(Reilly, 1995). Although the
activity of the gastrocnemius in C. calyptratus was variable, the
peroneus generally had a similar pattern of activity as that of S.
clarki. However, the morphology of the foot and ankle of C.
calyptratus differs substantially from a generalized lizard. Activation
of the peroneus while the foot of C. calyptratus is anchored to the
perch could move the knee away from the body and in an anterior direction,
thus flexing the ankle during early stance
(Fig. 2).
The appendicular anatomy of C. calyptratus differs considerably from that of Varanus, Dipsosaurus, and Sceloporus. However, the major features in the timing of muscles in common to these lizard taxa when moving on a level surface appear similar.
Effects of incline on chameleons
The hindlimb kinematics of C. calyptratus changed very little with
changes in incline, whereas the amplitudes of muscle activity changed
substantially. Moving uphill requires an increase in propulsive forces
compared to the level, because of the increased component of gravity opposing
the direction of movement. One method that chameleons use to propel their body
during the first half of stance is to flex their knee. The activity of both
the flexor tibialis externus and the puboischiotibialis of C.
calyptratus increased substantially while moving uphill compared to
level, and their peak amplitude occurred immediately following footfall. Thus,
these two muscles are probably the most important for early knee flexion and
for pulling the body forward. The activity of the caudofemoralis increased
when moving uphill, and probably contributes to knee flexion, but the peak
amplitude occurred after the knee began to flex at footfall and may be better
correlated with the role in long axis rotation of the femur for propelling the
chameleon uphill.
Moving downhill requires less propulsive force (compared to level locomotion) because of the increased component of gravity contributing to forward movement, but some muscles must actively resist the passive flexion of joints in order to maintain posture and control speed. Early knee flexion during stance can occur passively, and in order to prevent the joint from collapsing, a knee extensor should be active. For the first 20% of the stride cycle, the relative amplitude of the iliotibialis was slightly greater on the downhill compared to both the level and the uphill surfaces in C. calyptratus (Fig. 3), and it extends the knee. Thus, the iliotibialis may help prevent knee flexion when moving downhill. The iliotibialis also extends the knee during the second half of swing, and the relative amplitude of this burst of muscle activity increased markedly on uphill surfaces. Perhaps this increased amplitude of swing-phase activity reflects an increased force requirement for knee extension because of greater torque on the lower limb with the change in limb orientation.
The activity of the hindlimb muscles of C. calyptratus changed markedly with incline, supporting the idea that animals modulate the activity of muscles as the demands in the environment change. However, the primary form of modulating muscle activity was changing amplitude rather than timing relationships. Furthermore, the most conspicuous changes in amplitude that we found were for propulsive muscles, which increased in activity on an uphill surface and decreased in activity on a downhill surface. The lack of significant changes within an incline for the cross-correlations between most pairs of muscles (Table 3) further supports the conclusion that, despite changes in the intensity of muscle activity, the shape of the bar graphs indicating the relative timing of peaks and periods of minimal or no activity changed very little with incline for most muscles. Consequently, the synergistic or antagonistic relationships between pairs of muscles were usually not affected by incline. The most notable exceptions to the overall preservation in the relative timing of peak activity within a muscle were for the flexor tibialis externus and the puboischiotibialis on the downhill incline compared to the other two surfaces (Fig. 3). In contrast to conspicuous peak of activity in early stance for these two muscles on the level and uphill surfaces, such peaks were absent on the downhill incline. Thus, these two muscles were involved in the only cases where the cross-correlations between pairs of muscle activity changed significantly with incline.
Inclines and other vertebrates
All previous EMG studies on the effects of incline on vertebrate locomotion
are for mammals and birds (Pierotti et
al., 1989; Roy et al.,
1991
; Roberts et al.,
1997
; Carlson-Kuhta et al.,
1998
; Smith et al.,
1998
; Galbaldon et al., 2001;
Gillis and Biewener, 2002
;
Daley and Biewener, 2003
).
During level locomotion in cats, the knee and ankle joints flex briefly after
footfall and then extend throughout stance
(Carlson-Kuhta et al., 1998
).
However, flexion of the knee and ankle is absent during the stance phase of
cats on uphill grades. At paw liftoff on level and uphill surfaces, both the
knee and ankle of cats flex substantially for more than half of swing and then
extend prior to footfall (Carlson-Kuhta et
al., 1998
).
Hip extension in mammals serves a similar function to femur retraction and
rotation in sprawling-limbed vertebrates, since all of these movements tend to
advance the hip forward relative to the point of foot contact. In cats, the
hip begins to extend immediately after footfall regardless of incline
(Carlson-Kuhta et al., 1998;
Smith et al., 1998
), and the
amplitude of activity of stance-phase muscles that extend the hip (propulsive
muscles) increases when moving uphill compared to the level
(Pierotti et al., 1989
;
Carlson-Kuhta et al., 1998
).
The propulsive muscles of C. calyptratus are ones that flex the knee
for the first half of stance, extend the knee in the second half of stance,
and retract and rotate the femur throughout stance, and these muscles
increased in activity when moving uphill as compared to level
(Fig. 3). Thus, a common
response among distantly related groups of vertebrates is to increase the
recruitment intensity of propulsive-phase muscles when moving uphill. These
results are further supported by a study of rats, where the activity of the
biceps femoris (hip extensor and knee flexor) and vastus lateralis (knee
extender) muscles were the highest moving uphill
(Gillis and Biewener,
2002
).
During downhill locomotion, the activity of stance-phase muscles of cats
that extend the hip to propel the body decreases
(Smith et al., 1998). The
muscles involved in propulsion in C. calyptratus also decrease in
activity when moving downhill as compared to level locomotion
(Fig. 3). The muscles that flex
the hip, and thus prevent forward movement, have increased activity when the
cats move downhill (Smith et al.,
1998
). During downhill locomotion, the rectus femoris muscle in
cats, which extends the knee, also has increased activity
(Smith et al., 1998
).
Additionally, the timing of the onset of rectus femoris activity occurs
earlier in stance for downhill locomotion compared to level locomotion. Thus,
cats prevent the collapse of the knee joint when moving downhill both by
increasing the amplitude of activity of the rectus femoris and by shifting the
timing of activity.
Not all increases in EMG amplitude are associated with the need to increase
propulsion when moving uphill. For example, during uphill locomotion the
iliopsoas of cats flexes the hip and lifts the limb during swing, and this
muscle has increased activity compared to level locomotion
(Carlson-Kuhta et al., 1998).
The iliotibialis of C. calyptratus is, in part, a swing-phase muscle
that extends the knee, and it had increased activity when moving uphill during
swing compared to the level. When moving uphill the limb is more nearly
perpendicular to gravity, and this increases the torque, resulting in an
increase in activity of some swing-phase muscles in order to extend the
knee.
During uphill locomotion, the most anterior and posterior positions of the
limb during the entire stride in cats shift posteriorly compared to level
locomotion, resulting in a reduction of the anterior placement of the paw at
footfall relative to the hip (Carlson-Kuhta
et al., 1998). On both uphill and level surfaces, cats have
asymmetric longitudinal excursions of the foot relative to the hip, in which
the magnitude of posterior placement exceeds that of anterior placement
(Carslon-Kuhta et al., 1998), but this asymmetry is greater on the uphill.
Similarly, in Dipsosaurus dorsalis, the most anterior position of the
foot is less than the most posterior position relative to the hip, and the
most posterior position increases when moving uphill versus moving on
a level surface (Jayne and Irschick,
1999
). The most anterior (Xmax) and posterior
(Xmin) positions of the ankle relative to the hip in
C. calyptratus are unaffected by incline
(Higham and Jayne, 2004
).
Furthermore, rather than having marked asymmetry in longitudinal positions
relative to the hip, the maximum anterior distance of the ankle closely
approximated the maximum posterior distance of the ankle in C.
calyptratus, further supporting the idea that chameleons pulling their
body forward in early stance contributes to propulsion.
For generalized terrestrial lizards, the hindlimb kinematics change with
speed in a manner that increases the muscle strain of the caudofemoralis
(Nelson and Jayne, 2001). Such
increased muscle strain is commonly correlated with increased power
requirements for diverse vertebrate musculoskeletal systems performing a
variety of tasks. For example, muscle fascicles of running turkeys actively
shorten on an uphill surface, whereas they they have isometric activity on a
level surface (Roberts et al.,
1997
). Furthermore, the strain of some muscles while they are
active in rats is greater on the uphill than on the level surface
(Gillis and Biewener, 2002
).
The hindlimb kinematics of cats, generalized lizards, and most vertebrates
change considerably when moving on inclines
(Carlson-Kuhta et al., 1998
;
Smith et al., 1998
;
Jayne and Irschick, 1999
). In
contrast, the kinematics of C. calyptratus change minimally with
incline and may indicate that power output is modulated primarily by altering
force rather than strain during muscle activity.
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Ashley-Ross, M. A. (1995). Patterns of hind limb motor output during walking in the salamander Dicamptodon tenebrosus, with comparisons to other tetrapods. J. Comp. Physiol. A 177,273 -285.
Biewener, A. A. (2002). Future directions for the analysis of musculoskeletal design and locomotor performance. J. Morphol. 252,38 -51.[CrossRef][Medline]
Carlson-Kuhta, P., Trank, T. V. and Smith, J. L.
(1998). Forms of forward quadrupedal locomotion. II. A comparison
of posture, hindlimb kinematics, and motor patterns for upslope and level
walking. J. Neurophysiol.
79,1687
-1701.
Cartmill, M. (1974). Pads and claws in arboreal locomotion. In Primate Locomotion (ed. F. A. Jenkins), pp. 45-83. New York: Academic Press.
Daley, M. A. and Biewener, A. A. (2003). Muscle
force-length dynamics during level versus incline locomotion: a
comparison of in vivo performance of two guinea fowl ankle extensors.
J. Exp. Biol. 206,2941
-2958.
Farley, C. T. (1997). Maximum speeds and
maximum power outputs in lizards. J. Exp. Biol.
200,2189
-2195.
Farley, C. T. and Emshwiller, M. (1996).
Efficiency of uphill locomotion in nocturnal and diurnal lizards.
J. Exp. Biol. 199,587
-592.
Gabaldon, A. M., Nelson, F. E. and Roberts, T. J. (2001). Gastrocnemius muscle mechanics in turkeys during uphill and downhill running. Am. Zool. 41, 1448.
Gatesy, S. M. (1990). Caudofemoral musculature and the evolution of theropod locomotion. Paleobiol. 16,170 -186.
Gatesy, S. M. (1997). An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion. J. Morphol. 234,197 -212.[CrossRef]
Gillis, G. B. and Biewener, A. A. (2002).
Effects of surface grade on proximal hindlimb muscle strain and activation
during rat locomotion. J. Appl. Physiol.
93,1731
-1743.
Higham, T. E. and Jayne, B. C. (2004).
Locomotion of lizards on inclines and perches: hindlimb kinematics of an
arboreal specialist and a terrestrial generalist. J. Exp.
Biol. 207,233
-248.
Huey, R. B. and Hertz, P. E. (1982). Effects of body size and slope on sprint speed of a lizard Stellio (Agama) stellio. J. Exp. Biol. 97,401 -409.
Irschick, D. J., Austin, C. C., Petren, K., Fisher, R. N., Losos, J. B. and Ellers, O. (1996). A comparative analysis of clinging ability among pad-bearing lizards. Biol. J. Linn. Soc. 59,21 -35.[CrossRef]
Irschick, D. J. and Jayne, B. C. (1998).
Effects of incline on speed, acceleration, body posture, and hindlimb
kinematics in two species of lizard, Callisaurus draconoides and
Uma scoparia. J. Exp. Biol.
201,273
-287.
Irschick, D. J. and Jayne, B. C. (1999a). A field study of effects of incline on the escape locomotion of a bipedal lizard, Callisaurus draconoides. Physiol. Biochem. Zool. 72,44 -56.[CrossRef][Medline]
Irschick, D. J. and Jayne, B. C. (1999b).
Comparative three-dimensional kinematics of the hindlimb for high-speed
bipedal and quadrupedal locomotion of lizards. J. Exp.
Biol. 202,1047
-1065.
Jayne, B. C. (1988). Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta. J. Exp. Biol. 140, 1-33.[Abstract]
Jayne, B. C., Bennett, A. F. and Lauder, G. V. (1990a). Muscle recruitment during terrestrial locomotion: how speed and temperature affect fibre type use in a lizard. J. Exp. Biol. 152,101 -128.
Jayne, B. C., Lauder, G. V. and Reilly, S. M. (1990b). Short communication: the effect of sampling rate on the analysis of digital electromyograms from vertebrate muscle. J. Exp. Biol. 154,557 -565.[Medline]
Jayne, B. C. and Ellis, R. V. (1998). How inclines affect the escape behaviour of a dune-dwelling lizard, Uma scoparia. Anim. Behav. 55,1115 -1130.[CrossRef][Medline]
Jayne, B. C. and Irschick, D. J. (1999).
Effects of incline and speed on the three-dimensional hindlimb kinematics of a
generalized iguanian lizard (Dipsosaurus dorsalis). J.
Exp. Biol. 202,143
-159.
Lauder, G. V. (1994). Homology, form, and function. In Homology: The Heirarchical Basis of Comparative Biology (ed. B. K. Hall), pp. 151-196. San Deigo: Academic Press.
Lauder, G. V. and Shaffer, H. B. (1988). Ontogeny of functional design in tiger salamanders (Ambystoma tigrinum): are motor patterns conserved during major morphological transformations? J. Morphol. 197,249 -268.
Mivart, S. G. (1870). On the myology of Chamaeleon parsonii. Proc. Zool. Soc. Lond. 1870,850 -889.
Nelson, F. E. and Jayne, B. C. (2001). The effects of speed on the in vivo activity and length of a limb muscle during the locomotion of the iguanian lizard Dipsosaurus dorsalis. J. Exp. Biol. 204,3507 -3522.[Medline]
Peters, S. E. and Goslow, G. E., Jr (1983). From salamanders to mammals: continuity in musculoskeletal function during locomotion. Brain Behav. Evol. 22,191 -197.[Medline]
Peterson, J. A. (1984). The locomotion of Chamaelea (Reptilia: Sauria) with particular reference to the forelimb. J. Zool., Lond. 202, 1-42.
Pierotti, D. J., Roy, R. R., Gregor, R. J. and Edgerton, V. R. (1989). Electromyographic activity of cat hindlimb flexors and extensors during locomotion at varying speeds and inclines. Brain Res. 481,57 -66.[CrossRef][Medline]
Reilly, S. M. (1995). Quantitative electromyography and muscle function of the hind limb during quadrupedal running in the lizard Sceloporus clarkii. Zool. Anal. Complex Syst. 98,263 -277.
Roberts, T. J., Marsh, R. L., Weyland, P. G. and Taylor, C.
R. (1997). Muscular force in running turkeys: The economy of
minimizing work. Science
275,1113
-1115.
Roy, R. R., Hutchison, D. L., Pierotti, D. J., Hodgson, J. A.
and Edgerton, V. R. (1991). EMG patterns of rat ankle
extensors and flexors. J. Appl. Physiol.
70,2522
-2529.
Russell, A. P. (2002). Integrative functional morphology of the gekkotan adhesive system (Reptilia: Gekkota). Integr. Comp. Biol. 42,1154 -1163.
Russell, A. P. and Bauer, A. M. (1992). The m. caudifemoralis longus and its relationship to caudal autotomy and locomotion in lizards (Reptilia: Sauria). J. Zool., Lond. 227,127 -143.
Schmitt, D. (1998). Forelimb mechanics during arboreal and terrestrial quadrupedalism in Old World monkeys. In Primate Locomotion: Recent Advances (ed. E. Strasser, J. Fleagle, A. Rosenberger and H. McHenry), pp.175 -200. New York: Plenum Press.
Smith, J. L., Carlson-Kuhta, P. and Trank, T. V.
(1998). Forms of forward quadrupedal locomotion. III. A
comparison of posture, hindlimb kinematics, and motor patterns for downslope
and level walking. J. Neurophysiol.
79,1702
-1716.
Smith, K. K. (1994). Are neuromotor systems conserved in evolution? Brain Behav. Evol. 43,293 -305.[Medline]
Snyder, R. C. (1954). The anatomy and function of the pelvic girdle and hindlimb in lizard locomotion. Amer. J. Anat. 95,1 -46.[Medline]
Swanson, S. C. and Caldwell, G. E. (2000). An integrated biomechanical analysis of high speed incline and level treadmill running. Med. Sci. Sports Exer. 32,1146 -1155.[Medline]
Wainwright, P. C., Sanford, C. P., Reilly, S. M. and Lauder, G. V. (1989). Evolution of motor patterns: aquatic feeding in salamanders and ray-finned fishes. Brain Behav. Evol. 34,329 -341.[Medline]
Wickler, S. J., Hoyt, D. F., Cogger, E. A. and Hirschbein, M.
H. (2000). Preferred speed and cost of transport: the effect
of incline. J. Exp. Biol.
203,2195
-2200.
Zaaf, A., Van Damme, R., Herrel, A. and Aerts, P.
(2001). Spatio-temporal gait characteristics of level and
vertical locomotion in a ground-dwelling and a climbing gecko. J.
Exp. Biol. 204,1233
-1246.
Zar, J. H. (1996). Biostatistical Analysis. Upper Saddle River, New Jersey: Prentice Hall.