Ontogenetic development of locomotion in small mammals - a kinematic study
Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität, Erbertstr. 1, 07743 Jena, Germany
e-mail: nadja.schilling{at}uni-jena.de
Accepted 29 August 2005
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Summary |
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Despite their different life histories, the development of kinematic parameters in the altricial tree shrew and the precocial cui are surprisingly similar. General limb design, performance, and timing of segment and joint movements in the young animals were similar to adults in both species, even from the first steps. Touch-down of the forelimb occurred at the position below the eye in all individuals and limb position was highly standardized at touch-down; no major changes in segment and joint angles were observed. Significant changes occurred at lift-off. With increasing body mass, limb segments rotated more caudally, which resulted in larger limb excursions and relatively longer steps. Developmental changes in locomotor abilities were similar in both species; only the time necessary to reach the adult performance was different. Despite the widely assumed maturity of locomotor abilities in precocial young, the first steps of the cui juveniles were not similar to the movements of adults. The adult locomotor pattern was reached within the first postnatal week in the cui and by the time they leave the nest in the tree shrew (39 days after birth; individual P39).
These results suggest that during the evolution of precocial development only processes independent of exercise or gravity can be shifted into the intrauterine period. However, development of locomotor ability dependents on exercise, and adjustments and training occur during growth. Therefore, only the time necessary to reach maturity was clearly shortened in the precocial juvenile relative to the ancestral altricial condition.
Key words: altricial, precocial, postnatal, limb movement, symmetrical gait, X-ray, tree shrew, Tupaia glis, cui, Galea musteloides
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Introduction |
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The functional correspondence of limb elements has changed because of the
transition from the two-segmented limb design in reptiles to three-segment
limbs in mammals. In symmetrical gaits, the scapula corresponds functionally
to the femur, the humerus to the shank and the lower arm plus hand to the foot
(Fischer, 1994;
Fischer et al., 2002
). These
three limb segments are arranged in a zigzag configuration in the basic
therian limb (Fischer and Witte,
1998
). Vertical fluctuations of the body centre of mass and
torsions along the body axis can be avoided by using these double flexed
pendulums. Most of the limb displacement is caused by movements of the
proximal segments. The distal segments contribute less to total step length.
Pivots of the fore- and hindlimbs (scapular fulcrum and hip joint) are at
nearly the same height, resulting in similar functional pendulum lengths. At
touch-down, the femur is positioned parallel to ground and at lift-off the
humerus and shank are nearly horizontal. Because of the evolutionary `new'
functional correspondence of limb segments of the mammalian fore- and
hindlimbs, and despite the serial homologies, the kinematics of the shoulder
blade must be compared with the femur, the humerus with the shank, and the
lower arm and hand with the foot and toes.
All previous studies were undertaken on adult animals. Therefore, the
question arose as to whether these characteristics of basic limb design and
performance change during ontogenetic development. Ontogenetic studies of
kinematic parameters of mammals are rare. Developmental changes in limb
position have been described only for Rattus norvegicus and Felis
catus f. domestica (Peters,
1983; Westerga and
Gramsbergen, 1990
; Jamon and
Clarac, 1998
; Howland et al.,
1995
). Changes in hindlimb joint angles during development were
investigated in Cercopithecus aethiops
(Vilensky and Gankiewicz,
1989
). These studies utilized normal video recordings in which
limb movements, especially of proximal limb segments, are hidden under fur,
skin, soft tissues and muscles. Cineradiography is the only tool that allows
accurate analysis of limb segment and joint movements. This study is the first
attempt to analyse limb movements during ontogenetic development using
cineradiography.
Because altricial and precocial development could result in different
patterns of limb use during postnatal growth, two species were chosen for
analysis. The tree shrew Tupaia glis gives birth to typical altricial
juveniles, whereas the cui Galea musteloides has precocial young that
walk immediately after birth. Only the kinematic changes of symmetrical gaits
were studied, because the walk and trot arise first during ontogeny in
different mammalian species independent of their preferred gait as adults
(Felis catus f. domestica:
Peters, 1983; Bradley and
Smith,
1988a
,b
;
Rattus norvegicus: Altman and
Sudarshan, 1975
; Geisler et
al., 1993
; Macaca fuscata:
Nakano, 1996
; Gerbillus
dasyurus: Blumberg-Feldman and Eilam,
1995
; Jaculus orientalis:
Eilam and Shefer, 1997
;
Microtus socialis, Meriones tristrami, Eliomys melanurus:
Eilam, 1997
). The aims of the
present study were to investigate the development of locomotion in order to
describe the process by which the adult pattern of locomotion emerges and to
determine the time of onset of adult limb performance.
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Materials and methods |
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The species were selected because of their comparable body size, similar
adult kinematics and different reproductive biology. Although the two species
differ in their habitats, cuis living underground in open grasslands while
tree shrews are arboreal, both species have comparable limb design and
performance (Schilling and Fischer,
1999; Fischer et al.,
2002
). As Jenkins
(1974
) pointed out, for small
animals like tree shrews, tree branches are relatively thick and impose the
same demands for locomotion as does the ground in terrestrial species.
Locomotor differences resulting from the presence or absence of the tail in
the tailed tree shrew and tail-less cui were not addressed in the current
study, because differences in kinematics and dynamics between tailed and
tail-less species are only relevant to asymmetrical gaits such as the gallop
or half bound, in which extensive sagittal spine movements occur
(Schilling et al., 1999
;
Fischer et al., 2002
), or
during arboreal or non-level locomotion.
Limb kinematics of cuis were investigated in previous studies using a
different experimental set up (Fischer,
1999; Fischer et al.,
2002
). New data were collected to guarantee the use of the same
protocol for all subjects. Locomotor parameters of adult tree shrews from a
previous study, which included more detailed information about metric
parameters, footfall patterns, gait dependent kinematics, intervertebral
sagittal spine movements and intralimb timing, were included to increase the
sample size (Schilling and Fischer,
1999
).
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Kinematic recording
Limb movements were studied by high-speed-cinevideography (150 frames
s-1) recorded at the IWF Knowledge and Media gGmbH at
Göttingen, Germany (Fig.
1). The X-ray system consisted of an automatic X-ray source image
amplifier chain (Phillips 9807 501 800 01, Germany). Pulsed X-ray shots (57-82
kV, 200 mA) were applied. Images from walking animals in lateral perspective
were recorded from the image amplifier using one of three synchronous working
cameras of the high-speed video-system Camsys® (Mikromak Service K.
Brinkmann, Berlin, Germany; Fig.
1). The other two cameras recorded the animal's motion in cranial
and lateral perspectives to verify that the locomotion occurred parallel to
the image amplifier.
Animals walked on a horizontal motor-driven treadmill within a Perspex enclosure (100 cmx45 cmx11 cm). Treadmill speed was held relatively constant during X-ray shots (mean coefficient of variation of animal's speed: 0.19). No attempt was made to record either acceleration or deceleration; rather, animals moved at their preferred `travel speed'. Recording time was limited by the memory capacity of Camsys® (6.83 s). The size of the image amplifier (20 cmx15 cm) only allowed for synchronous recording of all four limbs in the younger and smaller animals. Fore- and hindlimbs had to be filmed separately in older animals. An orthogonal wire grid placed perpendicular to the projection plane and at the position of the animals sagittal plane while on the treadmill provided reference points for motion analysis and correction of geometric distortions.
Motion analysis
The analogue videotapes were converted using a video processing board
(`Screen machine I', FAST Multimedia AG, Munich, Germany). Of the video
sequences, only trials with continuous motion and several successive steps
were used. Since treadmill speed was held relatively constant during X-ray
shots, animals velocity was also nearly constant during a given sequence.
Skeletal landmarks were interactively captured and their x- and
y-coordinates used to define vectors for the calculation of metric
and kinematic parameters. Locations of captured skeletal landmarks are
illustrated in Fig. 2.
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Metric parameters were calculated as vertical (e.g. height of fulcra) and horizontal (e.g. step length) distances. Segment angles were calculated from the horizontal, and joint angles were calculated on the flexion side of each joint (Fig. 2). Mean touch-down and lift-off angles, effective angular movements, maximum and minimum segment and joint angles, and maximum joint excursions were determined and compared among individuals (Table 2). Mean touch-down and lift-off angles of all cuis and all juvenile tree shrews were correlated with body mass and age. Adult tree shrews were excluded, because their exact age was unknown. The regression coefficient (r) and confidence intervals were calculated to determine the extend to which the slope differed from zero.
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Segment and joint angles were projected onto the sagittal plane to
calculate their contribution to step length. The contribution of joint angular
movements to total step length was calculated by the `overlay method' (for
details, see Fischer and Lehmann,
1998; Fischer et al.,
2002
). The `overlay method' takes into account that displacements
of more proximal elements and vertical displacements of pivots during stance
contribute to segment displacements. Calculations were based on mean values of
selected, typical gait sequences; the stance and swing phases were normalized
to the same period using linear interpolation.
Mean heights of the fore- and hindlimb pivots were calculated. The pivot of the forelimb was assumed to lie where the scapular spine meets the vertebral border of the scapula. In the hindlimb, the hip joint was assumed to be the fulcrum. In order to compare the limb excursions at touch-down and lift-off among different age stages, the horizontal distance between the position of the limb's fulcrum and the touch-down or lift-off point were expressed as a percentage of the height of the limb's fulcrum (relative limb protraction and retraction, respectively).
Error evaluation
Optical distortion due to parallax and aspect ratio were automatically
corrected during frame-by-frame analysis. The accuracy of capturing skeletal
landmarks is affected by the contrast of bones due to differences in thickness
and calcification at different ages. The error of capturing skeletal landmarks
was tested by repeatedly marking all landmarks in five different frames, five
times, for the youngest animals and the adults of both species. Average
standard deviations (S.D.) of the mean values of
coordinates and angles indicate the error for marking landmarks. Error ranged
between 0.1 mm and 1.4 mm for x- and y-coordinates,
0.3-9.9° for segment angles, and 1.1-10.6° for joint angles. Joint
angle error is higher because the errors of adjacent segment angles may be
cumulative in joint angles. No differences between fore- and hindlimb
landmarks were found. Standard deviations were higher for younger animals with
thinner bones than for older ones. Within limbs, more gracile limb elements,
such as phalanges and scapular fulcra, are more prone to digitising errors
than robust long bones (e.g. humerus or femur).
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Results |
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General limb performance in juveniles was comparable to that of adults even during the first steps. Limbs were always arranged in the typical zigzag limb configuration. Limb segment and joint movements showed the same trajectories as in adults. Major changes in limb position during postnatal development occurred, and were especially noticeable at the end of stance phase.
Fulcra and limb position
In all animals, independent of age, fore- and hindlimb pivots (scapular
fulcrum and hip joint) were at the same height above the ground. During
locomotion, both pivots were held at nearly the same level; no drastic
vertical fluctuations occurred. During development, the vertical distance
between ground and limb pivots increased by one third in both species (tree
shrew: P14 34 mm, adult 47 mm; cui: P0 32 mm, adult 45 mm).
In order to compare limb's pro- and retraction between individuals of different body size at touch-down and lift-off, the limb pivots were scaled to the same vertical distance (100%) and the position of touch-down or lift-off was expressed as a percentage of the pivot's height (Fig. 3). In relation to the height of forelimb pivots, the horizontal distances between the limb pivot and the point of touch-down or lift-off were comparable in adults of both species (Fig. 3). In the tree shrew, this distance exceeded the height of the forelimb pivot by about 19%, resulting in a relative forelimb protraction of 119%, whereas relative limb protraction was much smaller in the cui (79%). Even in the youngest tree shrew, relative limb protraction at touch-down was higher (107%) than in all cuis under study. The position of forelimb touch-down was independent of body mass or age in both species and ranged between 101-126% in tree shrew and 43-78% in cui. No major changes in limb excursions at touch-down occurred during development. However, the horizontal distance between the scapular fulcrum and lift-off position doubled during development in both species (tree shrew: P14 53%, adult(1) 125%, adult(2) 100%; cui: P0 49%, adult(1) 78%, adult(2) 89%).
Independent of age and species, the horizontal distance between touch-down and hip joint position was less than the height of the hip joint. Distances ranged from 46-96% in tree shrew and 50-102% in cui. As in the forelimb, no changes in relative limb protraction at touch-down occurred during postnatal development; touch-down position was not correlated with age or mass. Lift-off position was significantly correlated with body mass in both species. In the course of development of the cui, the horizontal distance between the hip joint and point of lift-off doubled (P0: 58%, adult(1) 121%, adult(2) 124%), while in tree shrew, this distance increased by 50% (P14 111%, adult(1) 158%, adult(2) 177%).
Segment and limb joint performance
In general, segment and joint movements started at the end of one step
phase and continued into the next phase (for details of timing, see
Schilling and Fischer, 1999).
Therefore, the onset of protraction and retraction were not strictly coupled
to touch-down and lift-off events. Timing of segment and limb joint movement
was comparable to that in adults from the first steps of the youngest
animals.
Scapula
Scapular movements were composed of rotational and translational
components. Vertical and horizontal translations of the shoulder blade were
ignored in this study because of technical limitations of the resolution of
cinevideography. The scapular spine was used to indicate the orientation of
the shoulder blade. Retraction of the shoulder blade started shortly before
touch-down. Mean touch-down angles were similar in the adults of both species
(Table 3). During stance phase,
the shoulder blade rotated caudally to reach a maximum angle of 92-95° in
both species. The scapula was already protracted at lift-off, and therefore,
mean lift-off angles were smaller than maximal excursions. During swing phase,
the shoulder blade rotated cranially and reached a minimum angle of 32-38°
in both species just before touch-down.
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Mean touch-down angles of the juveniles were higher than those of adults in
both species, but were significantly correlated with age and body mass only in
cuis (r=0.54 and 0.51, respectively; P0.05). Mean
lift-off angles increased with age in tree shrews (r=0.59,
P
0.05) and with body mass in cuis (r=0.50,
P
0.05). The more protracted touch-down position of the scapula
combined with the decreased caudal rotation at the end of stance phase
resulted in lower effective angular movements in younger animals. Whereas the
minimum angle during stance phase and touch-down angle were the same in
adults, the minimum angle of stance was lower than touch-down angle until the
age of P25 in tree shrews, as well as in the underweight individual P39(2),
and until age P5 in cuis. Thus, the scapula was displaced cranially under load
after touch-down in juveniles but was held at a constant position in the older
animals.
Humerus
At touch-down, the humerus was held in a nearly vertical position in adult
tree shrews and much more retracted in adult cuis
(Table 3). During stance phase,
the humerus rotated caudally, crossed its horizontal position and reached its
minimum angle. Minimum angles in the adult cuis were slightly lower than in
adult tree shrews. Because of synchronous extensions of shoulder and elbow
joints at the end of stance, the humerus was rotated slightly cranially until
and after lift-off, and therefore minimum values of swing were lower than
lift-off angles. The humeral angle reached its minimum of swing phase within
the first third of swing phase. The maximum angle of swing was much higher in
the adult tree shrews and crossed the vertical line, but was much more
inclined caudally in the adult cuis and never reached a vertical orientation.
Because of the greater cranial excursion of the humerus, effective angular
movement and amplitudes were greater in adult tree shrews than in adult
cuis.
Although no significant changes in mean touch-down or lift-off angle were
observed during postnatal development of the cui, mean lift-off angle of the
humerus was correlated with body mass in the tree shrew (r=0.78,
P0.01). In younger individuals, humerus was rotated beyond the
horizontal position. Nevertheless, the humerus was rotated the same amount
dorsally at lift-off in each age stage. Adult values of mean lift-off angles
were observed for individuals larger than 121.0 g (P25) in the tree shrew.
Mean touch-down angle did not change during ontogeny in tree shrews. The
underweight tree shrew P39(2) was better classified with younger animals of
comparable body mass. Because of the smaller angle at lift-off and the
unchanged angle at touch-down, effective angular movement in juveniles
exceeded those of adult tree shrews.
Lower arm
Mean minimum angles of the lower arm at the end of swing phase were -1°
and -2° in adult tree shrews and 3° and 8° in adult cuis,
indicating a nearly horizontal position
(Table 3). Retraction of the
lower arm had already begun at touch-down. Therefore, mean touch-down angle
was higher than the minimum angle of swing phase. Maximum angular excursion
was reached at the end of stance phase, and slightly higher values were
observed in adult tree shrews than in adult cuis. Mean lift-off angles were
lower than maximum excursions, because protraction began before lift-off.
Effective angular movements were higher in adult tree shrews than in adult
cuis because of lower values at touch-down and higher values at lift-off.
In both species, changes in lift-off position of the lower arm were
observed, but no changes in the touch-down position were evident during
ontogeny. Lower arm angle at lift-off was correlated with age and body mass in
the cui (r=0.66 and 0.67, respectively; P0.01), but
lift-off angle was more correlated with age than with body mass in the tree
shrew (r=0.83, P
0.001 and 0.73, P
0.01,
respectively). Higher effective angular movements with increasing age or body
mass were caused by increased angles at lift-off. Angles of juvenile cuis
older than P5 were equivalent to those of adults. As in the humerus, all data
from the underweight tree shrew P39(2) were comparable to those of younger
individuals of the same body mass. Mean lift-off angle of the other tree shrew
of the same age was not significantly different from adult values. Minimum
angle during stance and angle at touch-down were similar in all age stages of
both species, such that no cranial displacement under loading was
observed.
Hand
Carpus and metacarpus were considered together as one segment. With a mean
touch-down angle of 10° and 14° in tree shrews, the hand was a bit
more declined in adult tree shrews than in adult cuis (24° and 28°)
(Table 3). During stance phase,
the palm was lifted from the ground into a digitigrade position and reached
its maximum angle of retraction at lift-off. After lift-off, caudal rotation
continued until the hand reached its maximum swing angle of 175-185° in
adults of both species. The subsequent protraction ended when the hand
attained minimal cranial rotation during swing phase. The hand crossed the
horizontal in adult tree shrews but never reached the horizontal in adult
cuis.
During postnatal development, no significant changes in the touch-down
position of the hand were observed in the tree shrew, while mean touch-down
angles decreased during development in the cui with age and body mass
(r=0.55 and 0.49, respectively; P0.05). The angle at
lift-off increased with increasing age and body mass in tree shrews
(r=0.74 and 0.73, respectively; P
0.01) and increasing
age in cuis (r=0.49, P
0.05). Mean angles at touch-down
and at lift-off of the normal weight juvenile tree shrew P39(1) were similar
to those of adults, while, these values of underweight individual of the same
age P39(2) were comparable to younger animals of the same mass.
Shoulder joint
Because of the higher protraction of humerus at the beginning of stance,
maximum extension of the shoulder joint before touch-down in adult tree shrews
(134° and 138°, mean angles for each individual) exceeded the values
of adult cuis (91° and 99°; Fig.
4A,B). This was also reflected in larger mean touch-down angles in
adult tree shrews than in adult cuis (tree shrew, 118° and 122°; cui,
84° and 89°). Flexion of the shoulder joint started before touch-down
and continued during stance phase until the minimum value was reached as the
hand passed the below the shoulder joint. Both species exhibited similar mean
minimum angle (56° to 67°). At the end of stance, the shoulder joint
extended a second time, while the elbow joint extended and the humerus was
rotated cranially. At lift-off, mean shoulder joint angles reached 88° and
75° in adult tree shrews and 58° and 75° in adult cuis. After
lift-off, the shoulder joint was flexed until its minimum during swing phase
(47° to 58°) and the subsequent extension continued until the end of
swing phase. Because of greater extension at the beginning of stance and
similar lift-off angles, adult tree shrews showed greater effective angular
movements and amplitudes than adult cuis.
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As in the humerus, no changes in mean touch-down or lift-off position
occurred with increasing age or body mass during the development of the cui.
In the tree shrew, touch-down position was not significantly correlated with
body mass or age, but mean lift-off angle increased with increasing body mass
(r=0.76, P0.01). By the age that young tree shrews leave
the nest P39(1), shoulder joint values were comparable to those of adults.
Mean values of the underweight tree shrew P39(2) were similar to those of
younger animals with the same body mass. Because of the smaller lift-off angle
of the shoulder blade and the more caudally rotated humerus in the tree shrew,
mean lift-off angle was smaller in younger animals than in adults. The
shoulder joint was more flexed in younger stages at lift-off. The smaller
angle at lift-off and unchanged touch-down angles resulted in higher effective
angular movements in tree shrew juveniles than in adults. Values of juvenile
tree shrews were comparable to those of adults by age P30. Higher amplitude
shoulder joint angles during stance and swing phase in juvenile tree shrews
resulted from stronger flexion and extension of the shoulder joint. Because of
similar touch-down and lift-off angles and comparable minimum and maximum
values of young and old cuis, effective angular movement and amplitudes were
nearly constant during development.
Mean shoulder joint angle in adult tree shrews plotted against step cycle shows biphasic joint movement including two flexions and two extensions (Fig. 4A,B). In the altricial tree shrew juveniles, shoulder joint movement was monophasic, but the typical biphasic joint angle pattern developed as body mass increased. Notice that the angular movement of the under nourished juvenile P39(2) was comparable to those of younger animals of similar mass. During the development of precocial cuis, this biphasic joint movement varied, but no change during development was evident.
Elbow joint
At touch-down, the elbow joint was held at a right angle in adult tree
shrews (92° and 90°; Fig.
4A,B). The elbow was more flexed in adult cuis, with mean
touch-down angles of 69° and 74°. During stance phase, the elbow was
first flexed to a mean minimum angle of 58° to 65° in both species, as
the hand passed below the fulcrum of the forelimb. Then the elbow joint
underwent extension until reaching maximum values of 145° and 120° in
adult tree shrews and 105° and 124° in adult cuis at the end of
stance. Flexion of the joint during swing phase began before lift-off and
therefore mean lift-off angles (tree shrew, 143° and 116°; cui,
93° and 117°) were less than maximum extensions. After minimum flexion
during swing phase (26-38°), the elbow joint extended until its maximum
was reached at the end of swing phase (tree shrew, 144° and 119°; cui,
93° and 116°). The following flexion phase lasted until the middle of
the subsequent stance phase.
Mean touch-down angle of the elbow joint was not correlated with body mass
or age in either species, i.e. no developmental changes in elbow joint angle
occurred during touch-down. Despite this, significant changes in mean lift-off
position were found. Whereas mean lift-off angles were more correlated with
body mass than with age in the tree shrew (r=0.84,
P0.001 and r=0.65, P
0.05, respectively),
mean lift-off angles were correlated equally well with body mass and age in
the cui (r=0.55 and 0.49, respectively; P
0.05). The
elbow joint was more flexed at lift-off in the youngest tree shrew individuals
(body mass below 100 g) than in the youngest cui individuals (joint angle of
about 90°). With increasing body mass, lift-off angles of juvenile tree
shrews exceeded those of young cuis. At the age they left the nest, joint
angles of tree shrews P39(1) were similar to those of adults. In cuis, there
were no major changes in elbow joint angle at lift-off after the first week of
life.
Wrist joint
At touch-down, the hand was simply a continuation of the lower arm in both
species (wrist joint angle, 176° to 185°). The wrist joint was
increasingly flexed from touch-down until mid-stance. The minimum angle
reached was 117° and 129° in adult tree shrews and 129° and
132° in adult cuis. The wrist joint subsequently extended when the palm
left the ground until the next swing phase. Mean lift-off angles were 198°
in adult tree shrews and 206° in adult cuis. After maximum wrist extension
during swing phase (tree shrew, 270° and 255°; cui, 268° and
260°), the wrist joint flexed during the short swing time before
touch-down. Mean minimum joint angle during swing phase was comparable between
both species (169° to 173°).
Wrist angle at touch-down and lift-off did not change with increasing body mass or age. Due to comparable touch-down and lift-off angles as well as minimum and maximum excursions, the effective and maximum angular movements of juveniles and adults were similar.
Pelvis
Because of the rigid connection between the pelvis and sacrum, all
observable `pelvic movements' were the result of small, additive,
intervertebral movements. During walking and trotting, `pelvic movements'
occur mainly around the dorsoventral and longitudinal axes of the pelvis
(lateral bending and tilting, respectively;
Jenkins and Camazine, 1977).
Sagittal vertebral movements resulting in pelvic protraction and retraction
are less pronounced during symmetrical gaits than during asymmetrical gaits.
Lateral bending and tilting could not be analysed, because of the
2D-projection of the X-ray. Therefore, only craniocaudal `pelvic movements'
were evaluated.
Position of the pelvis at touch-down was similar in adults of both species (Table 4). During stance phase, the pelvis moved caudally and was a bit more inclined at lift-off. Effective and maximal angular movements during stance and swing were very low in adults of both species (4° to 7° and 10° to 17°, respectively). During the development of the tree shrew, no change occurred in mean touch-down or lift-off position, or effective and maximal angular movements. Even from their first steps, juvenile pelvic angles were similar to those of adults. In the cui, however, the pelvis was more protracted during the locomotion of the youngest age stages. Mean pelvic angle at touch-down on the day of birth was only 130°, and it increased to 140° and 148° during development. Comparisons of effective angular movements during development showed that the pelvis was more inclined throughout the step cycle in the youngest animals. From P5, values varied individually, but were more or less similar to those of adults.
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Femur
The femur was almost horizontal at touch-down in adult tree shrews and cuis
(Table 4). The femur retracted
during stance phase, and reached its maximum excursion at the end of stance.
The femur was clearly more caudally rotated in adult tree shrews than in adult
cuis. As shown by its higher maximum excursion, the femur was held nearly
vertical during lift-off in the adult cuis (81° and 91°), whereas it
was much more retracted in the tree shrew (125°). Protraction of the femur
began shortly before lift-off and continued until the end of swing. The femur
rotated through the horizontal in some steps of adults of both species. Mean
minimum angle of swing was comparable between the adults of both species.
Femur retraction began before touch-down and continued until the end of
stance. Despite comparable cranial excursions, the effective and maximum
angular movements of femur in adult tree shrews exceeded that of cuis because
of greater caudal excursions.
Mean femur angle at touch-down was not significantly correlated with age or
body mass in either species. That is, touch-down position of the femur
remained unchanged during postnatal development. Lift-off angle increased with
increasing body mass in the tree shrew, however, the correlation was not
significant. In the cui, mean lift-off angles increased with increasing age
and body mass (r=0.72; P0.05). The smallest observed
mean lift-off angle of 36° was found in the newborn cui and the femur
angle at lift-off approached adult values after the first week of life. The
femur was never retracted past the vertical in young cuis below 50 g body
mass. In young tree shrews, the femur always passed through a vertical
position, but it was more retracted in the under nourished animal P39(2).
Adult values were not reached by the time the tree shrews left the nest
(Table 4). Effective angular
movements of the femur of juveniles were lower than those of adults, because
juveniles had smaller angles at lift-off, but a similar touch-down position.
Although the minimum femur angle during stance and touch-down angle were
similar in adults of both species, the minimum angle at touch-down was smaller
in the juveniles. This was due to passive cranial displacement of the femur
under load at touch-down in the younger animals. No passive protraction at
touch-down was observed after the age of P5 in cui and P25 in tree shrew.
Shank
The shank reached a minimum angle at the end of swing phase with mean
values of 60° and 59° in adult tree shrews and 51° in adult cuis.
Retraction of the shank started shortly before touch-down
(Table 4). Shank retraction
continued until the end of stance, reaching a more caudally rotated position
in the adults cuis than the adult tree shrews. The shank passed the horizontal
in both species. Minimum shank angle during stance phase was the same as mean
lift-off angle in the cui, whereas in the tree shrew, the shank was rotated
cranially until it reached a mean lift-off angle of -1° and -6°. That
is, the shank was positioned nearly horizontally at lift-off in adult tree
shrews and more inclined in cui. As the foot left the ground, the shank
continued retracting until it reached its minimum angle during swing. The
subsequent protraction continued until just before touch-down when the maximum
angle during swing phase was reached.
Mean touch-down position of the shank was independent of age or body mass
in both species. Touch-down angles were slightly higher than in older animals
only in the youngest cuis. Mean lift-off angle was horizontal in young cuis
and decreased significantly with age and body mass (r=0.57 and 0.53,
respectively; P0.05), while in tree shrews, shank angle increased
significantly with increasing age and body mass, approaching a more horizontal
position (r=0.88 and 0.87, respectively; P
0.001). By
P39, shank values of the normal weight animal were similar to those of adults,
while values of the underweight animal were comparable to younger individuals
of the same body mass.
Foot
Tarsus and metatarsus were analysed together as one segment. Touch-down
position was semi-digitigrade in adults of both species with a mean foot angle
of 9° and 14° in tree shrews and 14° and 19° in cuis
(Table 4). During stance, the
foot was retracted until it reached its maximum caudal rotation at lift-off.
Mean lift-off angles were comparable between the adults of both species. After
lift-off, which included a quick retraction of the foot, protraction began,
and continued until the end of swing phase. The foot was held horizontally in
some step cycles of adults of both species during swing phase. Mean minimum
angles ranged between 4° and -1° in adults of both species.
Whereas no change in touch-down position of the foot occurred during the
development of the tree shrew, mean touch-down angle decreased with increasing
age and body mass in the cui (r=0.58 and 0.60, respectively;
P0.05). Retraction of the foot at lift-off increased with age in
both species. Lift-off angle was positively correlated with age in the cui
(r=0.49, P
0.05) and more correlated with age than with
body mass in the tree shrew (r=0.82, P
0.001 and
r=0.78, P
0.01, respectively). Adult values were reached
after the first week of life in the precocial young of the cui and by the time
they left the nest in the altricial young of the tree shrew (P39). Effective
angular movements of the foot were lower in juveniles than in adults of both
species.
Hip joint
Mean touch-down angle of the hip joint was similar in adults of both
species (tree shrew, 35° and 30°; cui, 33° and 45°). During
stance, the hip joint extended and reached its maximum extension shortly
before lift-off (tree shrew, 145° and 144°; cui, 112° and
116°). Maximum angle during stance and mean lift-off angle of adult tree
shrews (141° and 142°) exceeded those of cuis (104° and 112°).
Flexion of the hip joint began at the end of stance and continued into the
following swing phase. Adults of both species had similar minimum hip joint
angles during swing phase (22° to 30°). The hip joint in adults of
both species was not flexed by loading at touch-down. Higher effective angular
movement in adult tree shrews than in adult cuis was due to greater extension
at the end of stance.
Whereas mean hip joint angle at touch-down decreased during development in
the tree shrew with increasing body mass (r=0.60;
P0.05), touch-down position was unchanged during development in
the cui. Mean lift-off angles were significantly correlated with age in the
tree shrew (r=0.60, P
0.05) and with age and body mass in
the cui (r=0.86 and 0.89, respectively; P
0.001). The hip
joint was increasingly extended at lift-off during development. Even in the
youngest tree shrews, mean lift-off angles exceeded those of adult cuis. By
P39, the hip joint was only slightly more flexed than in adult tree shrews.
With a mean lift-off angle of 112°, the hip joint of the underweight tree
shrew P39(2) was more flexed than that of any other tree shrew in this study.
After reaching 1 week old, values of precocial cui juveniles were comparable
to those of adults. A quick passive flexion in the hip joint at touch-down due
to loading was observed for the first three age stages of both species.
Therefore, mean touch-down angles and minimum angles during stance were not
the same in these individuals. Mostly due to the more flexed position of the
hip at lift-off, the effective angular movement of younger individuals was
lower than that of the adults in both species.
Knee joint
At touch-down, the knee joint was a little more extended in adult tree
shrews (65° and 59°) than in adult cuis (49° and 55°). During
stance, the knee was flexed to angles of 44° to 55° and extended until
just before lift-off. The knee joint of adult tree shrews reached extension
angles (126° and 121°) that were twice those of adult cuis (64°
and 75°). Consequently, mean lift-off angles in adult cuis (56° and
59°) were much lower than those of adult tree shrews (124° and
119°). Flexion of the hip joint during swing reached minimum angles of
42° and 33° in the adult tree shrews and 28° and 35° in the
adult cuis.
Mean knee angle at touch-down was not correlated with age or body mass in
the tree shrew. In contrast, mean touch-down angle decreased with increasing
age and body mass in the cui (r=0.55 and 0.49, respectively;
P0.05). Mean knee angle at lift-off was significantly positively
correlated with age and body mass in both species (tree shrew: r=0.56
and 0.68, P
0.05, respectively; cui: r=0.61 and 0.64,
P
0.01, respectively). Mean lift-off angles of the youngest tree
shrews exceeded those of all investigated stages of the cui. As in the hip
joint, the underweight tree shrew juvenile P39(2) had the lowest value at
lift-off of all the individuals studied (84°). Mainly due to significant
changes in lift-off angle, effective and maximum angular excursions increased
during ontogeny. Therefore, the knee joint was more extended at touch-down
than at lift-off in younger cuis until P9, when this relation was reversed. In
tree shrews, knee angles were always higher at lift-off than at
touch-down.
Ankle joint
At touch down, the ankle joint was similarly flexed in the adults of both
species (tree shrew, 58° and 62°, cui, 59° and 51°). During
the first half of stance phase, the ankle joint underwent dorsal flexion and
reached mean minimum angles which were similar in both species (47° to
50°). Extension of the ankle lasted until the end of stance phase and
maximum extension during stance and mean lift-off angle were nearly the same
in both species (tree shrew, 137° and 118°; cui, 98° and
103°). Higher values in adult tree shrews were due to greater plantar
flexion of the ankle joint at lift-off. Minimum angle during swing phase was
reached after lift-off (34° to 43°) and was followed by a short
extension. Flexion of the ankle joint started shortly before touch-down and
continued into stance phase. Effective and maximum angular movements of the
ankle joint were higher in adult tree shrews than in cuis because of greater
plantar flexion.
During postnatal development of the cui, mean touch-down angle decreased
with increasing age and body mass (r=0.57 and 0.56, respectively;
P0.05). Despite increasing dorsal flexion of the foot at
touch-down during development, lift-off position remained unchanged. The
opposite was true for the tree shrew. Although mean touch-down position of the
ankle joint was not significant correlated with age or body mass, mean
lift-off position increased with increasing age and body mass
(r=0.81, P
0.001 and r=0.78, P
0.01,
respectively). By P39 in the tree shrew and after the first week of life in
the cui, ankle position had reached adult values.
Summary of developmental changes in kinematics
Beginning with their first steps, all individuals had the typical zigzag
limb configuration of adults (Fig.
5). Furthermore, the general timing of segment and joint angle
movements did not change during development. Limb position at touch-down was
comparable to that of adults in the first steps of both species. In tree
shrews, only mean touch-down angle of the hip joint decreased with increasing
body mass during postnatal development. In cuis, mean touch-down angles of the
scapula, hand and foot, as well as knee and ankle joints, decreased with
increasing age or body mass. No other segment or joint angles changed during
development.
|
Contribution of segment movements to stance length
The contribution of each segment's movement to stance length depends on the
height of pivot, and the angular excursion and length of the segment.
Therefore, more proximal limb segments contribute more to forward displacement
than more distal ones (Table
5). Independent of age or body mass, the scapula and femur
contributed the highest percentage to stance length in both species. The
scapula contributed 34-46% of stance length in tree shrews and 44-60% in cuis.
Angular movement of the femur clearly contributed more to stance length in
tree shrews than in cuis (Table
5). Contributions to stance length by the distal elements were
independent of age and body mass and did not change during development in
either species. The angular excursion of the hand contributed 5-17% of stride
length in both species. In the hindlimb, the contribution of the phalanges to
stance length was very low in most individuals and zero in others (-18% to
-3%).
|
The contribution of the middle segments of the forelimb to stance length changed drastically during development. In both species, the contribution of the excursion of humerus to stance length decreased during development (tree shrew: from 44% at P14 to 18% in adults; cui: from 37% at P0 to 8% in adults). Whereas lower arm rotation did not contribute stride length in the youngest animals (tree shrew P14, 8%; cui P0, 1%), its contribution increased to one third of stance length by the end of the investigated developmental period. Despite these developmental changes in the forelimb, the contribution of foot rotation was one third of stance length irrespective of age or body mass in both species. Whereas shank movement contributed to stride length in young cuis, it did not contribute in older animals [P0 18%, adult (2) -4%]. The shank did not contribute to stance length in any tree shrew (-7% to -18%).
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Discussion |
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Segmental and joint movements of adults of different mammalian species
began at the end of stance or swing phase shortly before touch-down or
lift-off and lasted continuously into the next phase
(Fischer, 1994;
Schilling and Fischer, 1999
;
Fischer and Lehmann, 1998
;
Schmidt and Fischer, 2000
;
Fischer et al., 2002
). The
onset of protraction and retraction was not coupled to the events of
touch-down and lift-off. For instance, retraction of all limb segments started
in the last third of swing phase during symmetrical gaits. At lift-off, the
proximal limb segments (scapula and femur) were already in protraction
(Fischer et al., 2002
). From
birth, the timing of segment and limb joint movements was similar to that in
adults; no developmental changes in timing occurred. Leg retraction just prior
to ground contact is a common principle in animal locomotion. The effect of
leg retraction was employed with a conservative spring mass model
(Seyfarth et al., 2003
) but
also with biomechanical models for quadrupedal locomotion
(Herr et al., 2002
) in order
to test its effect on running stability. In all models, leg retraction could
significantly improve stability and swing-phase limb dynamics played an
important role in stabilisation of running animals
(Herr et al., 2002
;
Seyfarth et al., 2003
).
Touch-down position of almost all limb segments and joints was nearly
constant during postnatal ontogeny. The point of touch-down of forelimbs was
below the eye in all juveniles. Examinations of adults of different therian
species confirm the invariance of touch-down point and touch-down limb
position (Fischer et al.,
2002). Therefore, touch-down turns out to be the most standardized
event during locomotion in both juveniles and adults. Touch-down is a crucial
event during the step cycle because it is the moment that the body first comes
in contact with the ground and it is the beginning of limb support. Flexion of
the joints and foot placement are highly standardized at this crucial moment,
which possibly enables the animal to react to unexpected ground conditions.
The flexed limb can be further flexed or extended to adjust to unexpected
obstacles. In both adults (Fischer et al.,
2002
) and juveniles (this study), modulations of stride duration
and stride length took place primarily at lift-off, the less critical point in
the stride cycle. The highly standardized touch-down position is therefore
hypothesized as a `kinematic goal' of limb movement, which has to be reached
at the beginning of each stride cycle to ensure stability of the body and to
prevent torsions of the body axis. The uniformity of touch-down positions has
to be addressed in further studies in order to test this hypothesis.
Variable parameters
Major changes in limb position occurred at lift-off during locomotor
ontogeny. In both species, mean lift-off angles of the scapula, lower arm,
femur and foot increased during development. This resulted in higher
extensions at most limb joints as the animals matured. From the moment that
the phalanges passed below the elbow joint during stance, the flexors must
prevent passive extension of the elbow caused by gravity; EMG-activity of the
extensors (m. triceps brachii) is reduced in small mammals
(Fischer, 1999;
Scholle et al., 2001
). By
changing the activation of the flexors, the joints may be flexed or extended.
In juveniles, the lower arm and femur are held nearly vertically at lift-off.
Juveniles avoided large caudal limb excursions over the vertical position,
possibly because of weaker flexor muscles. Extensors are more mature than
flexors because they are used earlier in ontogeny to elevate the body
(Fox, 1964
). Higher tone in
extensor muscles than flexors was described in various species independent of
their life histories (Fox,
1963
). Early development of the extensors may be connected to fact
that the first steps of juveniles use the adult touch-down position.
Until age P5 in Galea musteloides and P25 in Tupaia glis
[except for P39(2)] a slight protraction of the scapula and humerus was
observed at touch-down. These movements could be passively evoked by gravity
during limb loading. Perhaps the muscle force of younger animals is not strong
enough to resist gravity, or the timing of muscle activity is immature. But as
Carrier (1983) pointed out for
Lepus californicus, some juveniles are able to produce relatively
larger forces, per unit body mass, than adults, leading to higher
accelerations in the juveniles. Therefore, immature muscle activity patterns
in juveniles such as increased latencies between bursts, irregular activation
patterns of muscles independent from the movement, co-activation of muscles,
or the activity level of a given muscle
(Geisler et al., 1996
;
Gramsbergen et al., 1997
,
1999
) are more likely
responsible for the protraction of both segments at ground contact.
Younger individuals of both species had higher scapular angles at
touch-down than older animals, which resulted in a more vertical position and
therefore lower forces required to maintain this position. Investigations of
the dynamics of forelimbs in small mammals, especially Galea
musteloides, showed that the resultant ground reaction force was oriented
caudal to the shoulder joint (Witte et
al., 2002). If it were assumed that the orientation of the ground
reaction force is similar in juveniles and adults at touch-down (no data are
available for small juvenile mammals), the ground reaction force would be
nearly parallel to the scapular spine. The length of the lever arm from the
scapular pivot to the ground reaction force is much shorter if the scapula is
oriented more vertically than if it is horizontal. Therefore, the muscle force
necessary to maintain the scapula's position during touch-down is less with
the more vertical orientation of the scapula in juveniles than with the more
inclined position in adults. The vertical orientation of the scapula at ground
contact (initiation of load, body mass) may be due to the immaturity of the
shoulder muscles.
Vilensky and Gankiewicz
(1989) and Howland et al.
(1995
) studied developmental
changes in the hindlimb movement of Cercopithecus aethiops and
Felis catus f. domestica using videos. With increasing age, flexion
at all limb joints decreased and the limbs became more erect. The greater
extension of hindlimb joints of Cercopithecus aethiops and Felis
catus f. domestica resulted in more erect limb posture than in the
smaller species studied here. Extensive studies of the developmental changes
in hindlimb kinematics during over ground locomotion in Rattus
norvegicus, using external markers, were reported by Westerga and
Gramsbergen (1990
,
1993a
,b
).
Mean lift-off angles at the knee and hip joints decreased during development.
In contrast, extension of limbs increased during the development of Tupaia
glis and Galea musteloides.
The limbs are mainly retracted during stance phase and protracted during
swing phase (Fischer et al.,
2002). While segment movements are exclusively monophasic, joint
movements can be biphasic containing two flexions and two extensions per
stride. Joint movements vary from species to species. Cercopithecus
aethiops showed monophasic shoulder joint movements
(Whitehead and Larson, 1994
)
while Felis catus f. domestica
(English, 1978
;
Boczek-Funcke et al., 1996
) and
Eulemur fulvus (Schmidt and
Fischer, 2000
) exhibit biphasic joint behaviour during symmetrical
gaits. In Tupaia glis, shoulder joint movements depended on gait
(Schilling and Fischer, 1999
).
Biphasic movements were observed during symmetrical gaits but were reduced to
monophasic movements at asymmetrical gaits. During postnatal development, the
monophasic movement of the shoulder joint exhibited by younger Tupaia
glis changed to the adult, biphasic pattern. No changes in joint
movements occurred during the development of the precocial Galea
musteloides.
A limb segment's relative contribution to stride length depends on its
angular excursion, the height of its pivot, and its length
(Fischer and Lehmann, 1998).
Comparison of the contribution of segment movement to step length clearly
showed that the proximal limb segments (scapula, femur) produced more than
half of total stride length during symmetrical gaits in adults
(Fischer et al., 2002
). This
was also true in the juveniles studied here. As a result of the increased
rotation of the lower arm during development, the contribution of the lower
arm increased to one third of stance length in both species. For the hindlimb,
a significant change in the contributions of the segments during development
only occurred in Galea musteloides. In younger cuis, the shank was
positioned nearly horizontally and, in this orientation, it contributed its
entire length to stride length. During development, the shank became more
inclined (<-20° in adults) and contributed less to stride length.
Reproductive biology
Different patterns of postnatal development have evolved in eutherian
mammals. Species range from the ancestral state of naked juveniles with closed
eyes and ears, completely dependent upon maternal care (e.g. rats, mice or
tree shrews), to the derived state of fully haired young, which feed
themselves and are capable of locomotor activity at birth (e.g. horses, hares
or cuis; Sánchez-Villagra and
Sultan, 2002).
Contrary to all expectations, the same developmental changes in limb
configuration and movement were found in both precocial and altricial species.
Only the time necessary for these developmental changes to occur was different
between the species. The adult kinematic pattern was reached after the first
week in the precocial young of the cui and by the time they would leave the
nest in the altricial juvenile tree shrews. During the evolution of precocial
development, only processes independent of exercise or gravity could be
shifted into the prenatal phase, such as the development of the overall
distribution pattern of muscle fiber types in limb muscles
(von Mering and Fischer, 1999;
Schilling and Fischer, 2001
;
N. S., personal observation). The development of locomotor ability is
dependent on use and gravity and must occur during postnatal growth.
Therefore, the same developmental changes were observed in both species.
Individuals of comparable age but different body mass were included in the
current study to test whether development is more dependent on chronological
age or on body mass. Differences in body mass were especially evident in the
tree shrew. In the majority of cases, developmental changes in kinematics were
more closely linked to body mass than to age. In particular, the underweight
juvenile tree shrew had kinematic parameters more similar to younger
individuals of the same body mass than to individuals of its age group.
Similar results were found in Rattus norvegicus and Ovis
aries (Yamaguchi et al.,
1993; Joubert,
1955
) and this is consistent with the work of Portmann
(1965
), who pointed out that
time is not an appropriate variable to choose when comparing developmental
stages.
Conclusions
Developmental changes were unexpectedly similar in the two species studied
here. Despite the advanced state of maturity at birth in the juvenile cuis,
the same kinematic parameters changed during postnatal development as in the
altricial juvenile tree shrews. The first steps of precocial juveniles were
not the same as those of adults. Adult kinematic parameters were reached after
1 week of age in young cuis, and by the time they would leave the nest in
juvenile tree shrews. A 1-week-old precocial cui is comparable in its
developmental maturity to a weaned altricial tree shrew (P39-41). The
postnatal time necessary to gain locomotor maturity in precocial young is one
third of the time necessary for the ancestral altricial state of mammalian
young. The development of locomotor ability depends on limb use and gravity
and therefore must occur in the postnatal phase. During the evolution of
precocial juveniles, this developmental period was clearly shortened.
Touch-down position of nearly all limb segments and joints was independent
of age or body mass in juveniles (this study) and of gait and velocity in
adults (Schilling and Fischer,
1999; Fischer et al.,
2002
; Witte et al.,
2002
), while lift-off position varied with speed and gait in
adults, and with age or body mass during development. As the moment of first
ground contact, touch-down position may be a kinematic goal that must be
reached at the beginning of each step cycle. Therefore, no major developmental
changes were found in the touch-down position. The earlier development of
extensors in comparison to flexors allows the animal to use adult touch-down
position in its first steps, while lift-off position changed as flexors
matured during postnatal ontogeny. Development of most kinematic parameters
depended more on mass than on chronological age, as demonstrated by the
addition of underweight individuals of certain age classes.
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Acknowledgments |
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