Basic limb kinematics of small therian mammals
1 Institut für Spezielle Zoologie und Evolutionsbiologie,
Friedrich-Schiller-Universität, Jena, Erbertstrasse 1, D-07743 Jena,
Germany
2 IWF Knowledge and Media gGmbH, Nonnenstieg 72, D-37075 Göttingen, PO
box 2351, Germany
* e-mail: b5fima{at}rz.uni-jena.de or fischer{at}pan.zoo.uni-jena.de
Accepted 12 February 2002
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Summary |
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Key words: in-phase gait, lumbar spine, locomotion, symmetrical gait, X-ray, small therian mammal
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Introduction |
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Our first aim is to present quantitative kinematic data of fore- and hindlimbs' movements for several, only distantly related, small therian mammals at different gaits. Based on this substantial amount of highly detailed work, a comparative study of limb configuration and kinematics was undertaken to look for basic kinematic similarities emerging together with the new therian limb. The principles that emerge from these studies, together with the published work especially on cats will be also tested for their validity in midsize ungulates.
Another key innovation of therian locomotion is the regular use of in-phase
gaits (gallop, half-bound, bound); crocodiles show gallop only exceptionally
as juveniles (Zug, 1974).
According to Hildebrand
(1985
), sagittal spine
movements occur typically in fast carnivores, lagomorphs, and rodents. We
present first data for other especially small therians. The consequences of
these `new' gaits on fore- and hindlimbs and especially lower spine kinematics
have never been quantified using cineradiography. Based on the X-ray study of
slow walking (i.e. exploratory walking) in the tree shrew Tupaia
glis, a restricted bending region of flexion between Th11 and L1 has been
described (Jenkins, 1974a
).
This observation will be tested in faster `in-phase' gaits. In our study, we
also included animals with and without tails, to test their influence on the
kinematics of the sagittal back movements.
Cineradiography is the only tool that recognizes the exact kinematics of
all proximal skeletal parts hidden under the skin and subcutaneous fat.
Previous studies on quadrupedal therian mammals quantitatively analysed either
(1) single joints such as the shoulder joint in rats (Rattus
norvegicus; Jenkins,
1974b), hip joint and back movements in the skunk (Mephitis
mephitis; Van de Graaff et al.,
1982
), trunk movements in the shrew-like opossum (Monodelphis
domestica; Pridmore,
1992
), elbow and wrist joint in the potto (Perodicticus
potto; Jouffroy et al.,
1983
), ankle joint in kangaroo rats (Dipodomys
spectabilis; Biewener and Blickhan,
1988
), single limbs at specific gaits (e.g. hindlimb in cats
Felis catus f. domestica;
Kuhtz-Buschbeck, 1994
), or (2)
qualitatively single steps only at one or more gaits (e.g. Tupaia;
Jenkins, 1974a
; jirds
Meriones shawi; Gasc,
1993
). Most data are available for the cat, which has long been
used as a model organism (Engberg and
Lundberg, 1969
; Goslow et al.,
1973
; Miller and Van der
Meché, 1975
; Jenkins
and Camazine, 1977
; Sontag et
al., 1978
; English,
1978a
,
b
,
1980
;
Halbertsma, 1983
;
Hoy and Zernicke, 1985
;
Caliebe et al., 1991
;
Kuhtz-Buschbeck et al., 1994
;
Boczek-Funcke et al., 1996
,
1998
,
1999
). From outside of our
group the only cineradiographic study on fore- and hindlimb kinematics at
different gaits was published by Rocha Barbosa et al.
(1996
) on the domestic guinea
pig Cavia porcellus.
Scapular displacement during quadrupedal locomotion has been measured in
Felis (Miller and Van der
Meché, 1975; English,
1978a
; Sontag et al.,
1978
; Boczek-Funcke et al.,
1996
), Rattus
(Jenkins, 1974b
),
Cavia (Rocha Barbosa et al.,
1996
), Virginia opossum, Didelphis marsupialis
(Jenkins and Weijs, 1979
) and
vervet monkeys Cercopithecus aethiops
(Roberts, 1974
;
Whitehead and Larson, 1994
).
The studies named describe a clear pro- and retraction of the shoulder blade
during locomotion, but the impact of this displacement on step length and the
overall kinematics of the forelimb has never been determined.
We have collected kinematic data on eight different small therian mammals
using cineradiography. Data of two phylogenetically distant metatherians
(Dasyuroides byrnei, Monodelphis domestica) and six eutherians
belonging to five different orders (Primates: Microcebus murinus;
Rodentia: Galea musteloides, Rattus norvegicus; Lagomorpha:
Ochotona rufescens; Hyracoidea: Procavia capensis;
Scandentia: Tupaia glis) are now available to elaborate upon the
kinematic principles of small mammal locomotion. In addition, data based on
analyses of two artiodactyls, Tragulus javanicus and the domestic
goat Capra hircus (Lilje and
Fischer, 2001), a very small rodent (Acomys cahirinus),
as well as another primate (Saguinus oedipus;
Schmidt and Voges, 2001
) are
included in this paper (e.g. in illustrating touch-down and lift-off
positions). Single kinematic studies including detailed information about
metric parameters, footfall patterns and gait-specific kinematics, as well as
intralimb timing are already published on Procavia capensis (Fischer,
1994
,
1998
), Ochotona
rufescens (Fischer and Lehmann,
1998
), Tupaia glis
(Schilling and Fischer, 1999
),
and Eulemur fulvus (Schmidt and
Fischer, 2000
). These published data are drawn together here by
further calculations, for example, on the contribution of limb segments to
step length.
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Materials and methods |
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Individuals were positively conditioned to move on a horizontal
motor-driven treadmill within a Plexiglas enclosure (length 100 cm, width and
height were adapted to the requirements of each species) except for the
arboreal quadrupedal Microcebus, which walked on a rope-mill, an
arboreal analogue of a treadmill. Treadmill speed was not fixed, but the
operator attempted to keep the running animal in front of the X-ray screen for
as long as possible. Thus, the operator adjusted the speed to obtain certain
preferred speeds of the animals. Comparisons of treadmill locomotion and
unrestrained locomotion have shown that the basic schemes of kinematics are
the same in both situations (Fischer,
1999).
Cineradiography
The X-ray equipment consisted of an automatic Philips® unit (Type 9807
501800 01) with one X-ray source image-amplifier chain. Pulsed X-ray shots
were applied (approximately 50 kV, 200 mA). The X-ray images on the image
intensifier were recorded either on 35 mm film using an Arritechno R35-150
camera or with a high-speed CCD camera (Mikromak Camsys®) operating at 150
frames s-1. The animals were filmed in a lateral projection with a
maximum exposure time of 10 s. As some of the animals were larger than the
area of interest covered by the image-amplifier (20.5 cmx15.0 cm), fore-
and hindlimbs were recorded separately. An orthogonal wire grid, perpendicular
to the projection plane, provided reference points for correction of
geometrical distortions and metrical calculations.
Processing of X-ray images
X-ray films were copied onto video tapes and A/D-converted using a video
processing board (Screen Machine® I, Fast® Multimedia AG, Munich,
Germany), and further analysed by application of the software `Unimark 3.6'
(by R. Voss). This software makes it possible to digitise interactively
previously defined landmarks with a cursor function; it also corrects
distortions automatically and calculate angles and distances. The positions of
digitised landmarks and angles calculated in the parasagittal plane are
illustrated in Fig. 1. Angles
calculated are the projections of angles onto the sagittal plane representing
their contribution to movements in the plane of forward motion.
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The errors generated by digitisation of skeletal landmarks and their influence on the angles calculated were tested by repetitive digitisation (five times) of one sequence (25 frames) for each species. The digitisation error depends on the size of the animal and the image contrast of skeletal elements. It ranges from 0.5° to 2.0° for segment angles (see below) and is roughly 1.0-3.0° for joint angles, because the errors of two adjacent segment angles combine in joints following the Gaussian rules of error propagation.
Analysis of angular movements and their contribution to step
length
Limb joint angles were defined anatomically and measured at the flexor side
of each joint. Segment angles were calculated versus the horizontal
plane. We shall use the term protraction (= cranial rotation) for the cranial
displacement of the distal end of each segment. Retraction (= caudal rotation)
describes its caudal displacement. Maximum amplitudes of joint excursion
during stance and swing phases were calculated from the initial moments of
segment and limb-joint movements. Effective angular displacements (EAD) were
defined as differences of angles at touch-down and lift-off. The ratio EAD
versus maximum joint amplitudes gives the coefficient of stance phase
(CSP). A ratio higher than 0.5 indicates a joint's action resulting in a
forward propulsive movement.
Fischer and Lehmann (1998)
proposed an `overlay method' to calculate the relative contribution of angular
movements to step length. While the CSP indicates the non-propulsive vertical
work of joints, only the overlay method enables calculation of the relative
contribution of segment movements to horizontal forward motion, because it
considers the displacements of pivots of the limb segments during stance
phase.
Summarising the `overlay method' in short, the calculations are based on mean values of typical gait sequences, of which stance and swing phase duration are scaled to equivalent relative durations using the method of linear interpolation. A polynomial fit of sixth order is used to interpolate data. For calculation, angular values are defined in the vertical plane to be positive if the distal end of the segment is in front of the proximal end. The horizontal distance (lp) between tip of toe and the pivot of the whole limb is determined for every single limb configuration during stance phase, using the lengths of segments and their angular excursions against the vertical plane. By overlaying the proximal segment onto the next configuration, without changing angles in the more distal joints, the difference between the horizontal excursion at instant i (lpi) and at instant i+1 (lpi+1) is the step length caused by the rotation of each particular segment. For each segment the absolute contribution to step length is given by the summation of all single-frame calculations in stance phase. Finally, the contribution of the remaining segments to forward motion is calculated in the same way, except for the subtraction of the angular movement achieved by the sagittal rotation of the more proximal segment(s). The relative contribution of segment displacement to step length depends on the pivot's height, the effective angular displacement (EAD) and the length of the segment.
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Results |
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Kinematic data comprise segment and joint angles at touch-down and lift-off, maximum amplitude of the stance phase, contribution of segment displacement to step length and the coefficient of stance for limb joints at symmetrical gaits (Tables 2A, 3A) and in-phase gaits (Tables 2B, 3B,C). Differences between trailing and leading limbs (first and second touch-down) were observed on the hindlimbs only at gallop and half bound and therefore, these limbs are presented separately.
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The following description of the kinematics of small mammalian locomotion is divided into three main parts: forelimb, spine movement, and hindlimb. The sections on limb kinematics start with the displacement pattern of the limb segments and their contribution to step length, followed by the description of joint movements.
Forelimb
Kinematics of forelimb segments
Segment displacements consist mainly of retraction during the stance phase
and protraction during the swing phase. In all species, retraction of all
segments starts before touch-down at 90-95 % of the previous step cycle
duration at symmetrical gaits and at 80 % of the previous step duration at
in-phase gaits (Fig. 2A,
B). Scapular protraction begins
at 85-90 % of stance duration at symmetrical gaits but its timing is more
variable at in-phase gaits. The beginning of humeral protraction varies around
lift-off at all gaits, whereas forearm protraction is timed to coincide with
lift-off at symmetrical gaits or with 10 % of swing duration at in-phase
gaits. Protraction of the hands begins late in the first third of swing. Fig.
2A,B
illustrates the high uniformity of segment displacements (except of the hand)
in all species.
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Forelimb protraction and retraction are executed mainly by scapular
displacement, as the most proximal segment. Retraction of the scapula begins
from the most flexed position at 35-40 ° in the late swing phase. Mean
touch-down angles of the scapula range within 37-51 ° at symmetrical gaits
and 42-54 ° at in-phase gaits. In those species in which symmetrical as
well as in-phase gaits could be analysed, an increased scapular touch-down
angle was observed at in-phase gaits. A continuous retraction of the scapula
leads to a nearly vertical orientation at the end of stance. Rotary movement
then stops and in aclaviculate species such as Procavia, a
translatory gliding along the thoracic wall follows (for details, see
Fischer, 1994). Mean scapular
lift-off angles are between 79 ° and 101 ° at symmetrical gaits and
are in approximately the same range at in-phase gaits
(Table 2A,B). Mean amplitudes
of scapular retraction are maximally 10 % higher than the differences of
angles at touch-down and lift-off. The greatest amplitude of scapular
retraction was measured in the rodents (60 ° for both species) and in
Monodelphis and Tupaia, each with 59 °.
In all species, humeral displacement is as uniform as scapular movement (Fig. 2A,B). Mean touch-down angles for five species are in a small range of less than 10 ° (58-65 ° at symmetrical gaits, 52-61 ° at in-phase gaits). Tupaia and Microcebus have a more protracted upper arm at touch-down with mean angles of 85 ° and 78 °, respectively (Fig. 4). In contrast, Dasyuroides has the most retracted humerus at touch-down, being only 36 ° at symmetrical gaits and 46 ° at in-phase gaits. This species also shows the lowest overall amplitude of humeral displacement at 59 ° and Tupaia the highest amplitude of humeral retraction at 105 ° (Table 2A). Retraction of the humerus starts before touch-down and is already completed at midstance. Afterwards, the humerus is positioned more or less horizontally and held in this position until the first quarter of the swing phase (Procavia -2 °, Galea -7 ° and Microcebus -5 ° at symmetrical gaits; Procavia 9 °, Galea -3 ° and Ochotona -1 ° at in-phase gaits). Monodelphis, Dasyuroides and Rattus elevate the humerus more above the horizontal line (mean angle between -18 ° and -21 ° at symmetrical gaits).
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The forearm is in matched motion with the scapula (i.e. both segments are displaced nearly parallel to each other), especially during the stance phase (Fig. 2B). Mean touch-down angle is highly uniform at symmetrical gaits and ranges between 24 ° and 36 ° with the exception of Tupaia (8 °) and Microcebus (11 °) in which by stronger protraction of the humerus and not by elbow flexion (see below) the forearm is placed almost parallel to the ground. At in-phase gaits, the mean touch-down angle is more variable within our sample of species and lies between 18 ° in Tupaia and 46 ° in Procavia. Retraction of the forearm continues until the end of stance phase and ends at lift-off at symmetrical gaits, or at 10 % of the swing phase at in-phase gaits. Lift-off angle varies slightly between species (107-122 °) at symmetrical gaits. Only Tupaia deviates from this position with a more retracted forearm (138 °) and thus has the greatest overall amplitude of forearm movement (133 °). The mean lift-off angle has a broader range at in-phase gaits. The lowest values were observed in Ochotona (96 °) and Tupaia (105 °), whereas Galea has the highest lift-off angle at 128 °.
The hand is placed in a semidigitigrad position; a digitigrad position was frequently observed only in Procavia. In Microcebus, walking on a rope-mill, the hand grasps around the circumference of the rope. Here, hand and wrist joint angles also were projected onto the sagittal plane. Hand displacements are highly variable between all species as compared to the relative uniformity of displacements of the more proximal segments. Mean touch-down angles vary within broad ranges (2-40° at symmetrical gaits, 4-52° at in-phase gaits). The highest angle value was measured in Procavia (Table 2A,B), in which the hand is displaced in a line with the forearm and synchronised with it at the start of retraction and protraction (Fig. 2A,B). Hand retraction starts in the second half of the stance phase and ends in the first third of the swing phase in all species except Procavia. Mean lift-off angles are between 78° (Microcebus) and 157° (Tupaia) at symmetrical gaits, but at in-phase gaits Tupaia (136°), are closer to the values observed in most other species (e.g. Galea 134°, Dasyuroides 130°, Procavia 132°). Monodelphis shows a relatively lower angle at these gaits (65°).
Contribution of forelimb segment movements to step length
The dissociation of segment and joint movements becomes obvious when the
displacement of humerus, forearm and hand are compared with the effective
angular movements in shoulder, elbow and wrist joints. Distal segments have a
low degree of proper motion in the proximal adjacent joint and are driven
passively by the action of the more proximal segments. For example, the proper
motion of the humerus in the shoulder joint of Microcebus during the
stance phase accounts for only 48% of its amplitude. More than 50% of its
humeral displacement results from scapular retraction alone and only 25% of
its forearm displacement is actually achieved in the elbow joint.
Calculation of the contribution of segment movements to step length using
the `overlay method' (Fischer and Lehmann,
1998) indicates the predominance of scapular retraction in
forelimb movement. Scapular retraction accounts for more than 50 % and up to
80 % for step length in most species but for less than 50 % in Tupaia
and Microcebus (Table
2A,B). The high value in Procavia (80 %) results from
both the high scapular pivot and the amplitude at in-phase gaits. In contrast,
the relative position of the scapular pivot in Dasyuroides is even
higher than in Procavia (Fig.
4) but the amplitude of scapular retraction is low and, therefore,
the overall contribution of the scapula is lower in Dasyuroides than
in Procavia.
The relatively lower scapular contribution in both Tupaia and Microcebus is due to an overall increase in step length, caused in the first instance by a stronger protraction of the humerus and additionally by an extensive retraction of the forearm in Tupaia. Except for these two species, the contribution of humeral displacement to step length is always less than half of the scapular amount. The forearm contributes positively to step length only in the second half of the stance phase when its pivot (the elbow) raises. The forearm's contribution can exceed the value of the upper arm in species in which the forearm is retracted extensively; e.g. Tupaia at symmetrical gaits or Galea at in-phase gaits. The hand contributes to step length only in the last third of the stance phase when the wrist joint is lifted from the ground; in most species it contributes approximately 5 % and never more than 10 % to step length.
Kinematics of forelimb joints
In almost all species, the shoulder, elbow and wrist joints display
biphasic angular movements during one step cycle for both symmetrical gaits
and in-phase gaits (except for the wrist in Procavia and the shoulder
in Tupaia; Fig.
2A,B).
Phase relationships between different joints indicate that extensions in the
shoulder, elbow and wrist joints are not synchronised. Flexion of all joints
starts before touch-down, causing retraction of the segments. Flexion in the
elbow joint reaches its maximum at 10-20 % of step duration (20-40 % of stance
duration) (Fig.
2A,B),
when the hand passes underneath the shoulder joint. Shoulder extension starts
at midstance. The maximal dorsiflexion of the hand is reached at 65-70 % of
stance duration. The second flexion of the shoulder joint coincides with the
beginning of scapula protraction at the end of the stance phase. The elbow
flexion initiates protraction of the forearms while maximum plantarflexion of
the wrist joint occurs only in the first half of swing phase. The shoulder
joint is the first joint to extend during the swing phase; elbow extension
then follows at 50 % of the swing duration or later. An earlier extension of
the elbow joint would counteract the forward movement of the limb. This
sequence of forelimb joint movements during one step cycle is observed
regularly in all species and at all gaits. Differences occur only in the
degree of flexions and extensions, not in the intralimb coordination
associated with the onset of movements.
In contrast to the amplitude of segment displacement, the amplitude of angular excursions in limb joints can be twice as high as the difference between the angles at touch-down and lift-off (effective angular displacement, EAD), especially in the elbow and wrist joint (Tables 2A,B). The coefficient of stance phase (CSP), calculated as the ratio of EAD and the amplitude of joint excursion, indicates the degree of horizontal versus vertical action of joints. A CSP value of less than 0.5 indicates mainly vertically stretching and bending of the limbs and not to body protraction.
The shoulder joint has a relative high CSP in all species. It ranges between 0.50 and 0.86 at symmetrical gaits and increases for most of the species at in-phase gaits (except for Procavia). Mean shoulder joint angles at touch-down range at symmetrical gaits from 75° in Dasyuroides to 123° in Tupaia, and are between 91° (Dasyuroides) and 132° (Tupaia) at inphase gaits (Table 2B). The mean lift-off angles are always smaller than touch-down angles and consequently, the resulting net joint movement of the shoulder joint is a flexion (except in Procavia at in-phase gaits). The variability of the lift-off angle is similar to that of the touch-down angle. In the first third of the stance phase, humeral retraction is faster than scapular caudal displacement, resulting in a flexion of the shoulder joint which ends at approximately 50 % of the stance duration. The flexion is rather weak in Procavia, Galea, Dasyuroides and Microcebus. Flexion diminishes at in-phase gaits, an effect which is pronounced in Monodelphis. Shoulder joint movement in Tupaia is exceptionally monophasic at inphase gaits, where the joint is continuously flexed during the whole of the stance phase and even until 26 % of swing duration (Fig. 2B). The lowest overall amplitude of shoulder movement was found at symmetrical gaits in Galea (23°) and at in-phase gaits in Procavia (23°), the highest in Tupaia (60°).
In almost all species, the amplitudes of elbow joint excursions during the stance phase occur within a small range (37-45°) at symmetrical gaits (Table 2A). Only the amplitude of the elbow joint of Tupaia (70°) deviates from these values, as a consequence of extensive retraction of the forearm at the end of the stance phase. At in-phase gaits, the amplitudes of elbow joint movements vary over a broader range, between 20° in Ochotona and 54° in Galea. Ochotona has both a reduced flexion at midstance and a reduced re-extension at the end of the stance phase (Fig. 2B). Compared to the shoulder joint, the net joint movement of the elbow joint is an extension in almost all of the animals we sampled at all gaits (except for Tupaia at in-phase gaits). The mean touch-down angle of the elbow joint is usually smaller than the lift-off angle and ranges from 71° in Dasyuroides to 93° in Galea at symmetrical gaits. At in-phase gaits, the lowest mean touch-down angle was measured in Monodelphis. In the other species, the mean angles increase to as much as 106° in Procavia. Compared to the shoulder and wrist joint, the mean touch-down angle of the elbow joint is more constant in all species and at all gaits. However, the range of the mean lift-off angle is higher (86-124° at symmetrical gaits, 89-127° at in-phase gaits). Tupaia shows the highest mean lift-off angles at symmetrical gaits (124°), whereas the highest lift-off angles in Procavia (127°) and Galea (125°) occur at in-phase gaits. The lowest angle (86°) was measured in Dasyuroides. The coefficient of stance of the elbow joint usually is lower than the CSP of the shoulder joint; mean values fall below 0.5 in Monodelphis, Dasyuroides, Rattus, Tupaia and Microcebus. In Ochotona and Procavia the CSP is 0.55. Only Galea shows a CSP of more than 0.6 at in-phase gaits.
The range of the mean CSP of the wrist joint is similar to that of the
elbow joint (Table 2A,B). The
coefficient of stance in most species is below 0.5 at symmetrical gaits
(0.25-0.45; Procavia 0.59), but it augments up to 0.36-0.65 at
in-phase gaits. The mean touch-down angle of the wrist joint ranges between
168-205° at symmetrical gaits, but all species except for
Procavia (175°) show a dorsiflexion of the wrist joint
(183-202°) at in-phase gaits. Procavia deviates from the other
species in our study by strongly reduced wrist joint excursions during the
stance phase at all gaits (Fig.
2A,B).
The hand is always displaced in line with the forearm owing to an anatomical
restriction in the wrist joint (Fischer,
1998). The wrist joint of the other species is extended most
during the last third of the stance phase, when the hand passes underneath the
elbow joint. The amount of extension is much higher at symmetrical gaits
(210-250°). Amplitudes of wrist joint excursion during the stance phase
decreases during in-phase gaits. Monodelphis is the only species that
extends the wrist joint to a similar degree (250°). The mean lift-off
angle varies between 154° (Tupaia) and 215°
(Microcebus) at symmetrical gaits and between 149°
(Tupaia) and 227° (Monodelphis) at in-phase gaits.
Spine movements
Sagittal spine movements are the result of additive flexions and extensions
between adjacent intervertebral joints in the lumbar vertebral column
(Fischer, 1994;
Fischer and Lehmann, 1998
) or
in the posterior thoracic and the lumbar vertebral column
(Schilling and Fischer, 1999
).
Previous reports of a limited region of flexion and extension between Th11 and
L1 in Tupaia (Jenkins,
1974a
) have been validated only for exploratory walks
(Schilling and Fischer, 1999
).
The additive effects of these movements lead to a displacement of the pelvis,
and are called `pelvic movements' in this study. Mobility within the
iliosacral joint was not observed. Cranial and caudal `pelvic' displacements
are pronounced at in-phase gaits (Fig.
3B,C),
in which the spine proves to be an important locomotory organ. Maximum cranial
displacement is reached late during the swing phase and the subsequent caudal
displacement continues until lift-off or even into the following swing phase.
Mean touch-down angles are particular high in tail-less species, showing a
nearly vertical pelvic position (e.g. Procavia, Ochotona). These
angles are lower in the tailed animals (e.g. Monodelphis, Tupaia). At
lift-off, the pelvis of tailed species is almost horizontal whereas in
tail-less animals the pelvis is more inclined. So, tail-less species start at
a more inclined position at the end of stance and reach an almost vertical
position at the end of the swing, whereas species with rather long tails
approach a horizontal position at lift-off but start much less inclined at
stance (Fig. 4). The tail-less
species Galea, however, behaves like the two latter ones. Despite
having different touch-down and lift-off angles, the effective angular
movement (about 40°) is comparable between all species, except for
Ochotona, which is more than 10° lower
(Table 3B,C). The mean
amplitude of the `pelvic movement' during the stance phase is also lowest in
Ochotona and highest in Procavia.
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At symmetrical gaits, two additional `pelvic movements' occur. The first, a
rotation about the dorsoventral axis, is caused by lateral additive
intervertebral joint movements (`lateral bending';
Jenkins and Camazine, 1977).
The second is a rotation about the longitudinal axis (`tilting';
Jenkins and Camazine, 1977
).
Because of the angle's projection into the sagittal plane, estimates of
lateral bending and tilting are difficult and were not attempted here.
Sagittal spine movements result in a low mean EAD of 3° and a mean
amplitude of 12° for all species at symmetrical gaits. The pelvis is held
virtually stable during locomotion (Fig.
3A). Pelvic position is inclined the most in Procavia
(51° at touch-down and 47° at lift-off) and more horizontal in
Tupaia and Galea (19° to 16°, and 22° to
19°). Mean pelvic angles of all other species are in the order of 35°
at touch-down and 32° at lift-off.
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Hindlimb
Kinematics of hindlimb segments
As in the forelimb, retraction of all hindlimb segments starts before
touch-down in the last third of the swing phase at symmetrical and in-phase
gaits. In particular `pelvic retraction' at in-phase gaits also starts at the
beginning of the stance phase and continues until the first quarter of the
swing phase in trailing and leading limbs of all species (but only the leading
limb of Procavia). Femoral retraction at symmetrical gaits ends after
95 % of the stance duration (Microcebus), at lift-off (Tupaia,
Rattus, Procavia) or during the first 10 % of the swing phase
(Monodelphis, Dasyuroides) (Fig.
3A). At in-phase gaits, femoral retraction is finished at lift-off
or during the first 15 % of the swing phase in trailing and leading limbs of
all species. Only in Ochotona, does retraction of the thigh start
before lift-off. In all species, protraction of the lower leg begins during
the first 35 % of the swing phase in both trailing and leading limbs; in
Procavia, however, it begins in the late stance phase. At symmetrical
gaits, lower leg retraction ends between 20-40 % of the swing phase in all
species. Although retraction of the foot comes to an end in the first third of
the swing phase in trailing and leading limbs of most species, but ends at the
lift-off in Procavia and in the late stance phase in the trailing
limb of Ochotona. Foot protraction starts in the first third of swing
phase in all species at symmetrical gaits.
Protraction and retraction of the hindlimb is executed mainly by femoral displacements at symmetrical gaits but by sagittal spine movements at in-phase gaits. At touch-down, the thigh is in an almost horizontal position in all species and at all gaits (7° at symmetrical gaits, -2° in trailing limb and -6° in leading limb at in-phase gaits). In species for which we have data for symmetrical and in-phase gaits, mean touch-down angles at in-phase gaits decrease to positions inclined above the horizontal. Fig. 4 illustrates the highly uniform thigh position that occurs, particularly at in-phase gaits. In comparison to touch-down, mean lift-off angles are more variable ranging from 51° in Dasyuroides and 125° in Tupaia at symmetrical gaits, as well as 47° and 101° in the trailing limb and 52° and 109° in the leading limb of Ochotona and Tupaia at in-phase gaits. The femoral retraction that follows ends with the maximum angle at left-off or in the first part of the swing phase. Mean amplitudes of femoral displacement increase from symmetrical to in-phase gaits in all species (except Tupaia) and are higher in the leading limbs than in the trailing limbs at in-phase gaits. The same mean amplitudes of both hindlimbs were only observed in Monodelphis at in-phase gaits, because animals performed half-bound gaits.
At symmetrical gaits, the lower leg is in almost vertical at touch-down in Microcebus, Procavia, Monodelphis and Rattus, but more caudally inclined in Dasyuroides, Tupaia and Galea (Fig. 4). From symmetrical gaits to in-phase gaits, mean touch-down angles increase in all species. At in-phase gaits, a nearly vertical position of the lower leg is realised in Monodelphis, Dasyuroides and Ochotona. Differences in this touch-down position were measured in Galea and Tupaia (which show a more posteriorly inclined lower leg) and in Procavia (in which the lower leg is more anteriorly directed in both trailing and leading limbs). In general, mean touch-down angles are comparable between trailing and leading limbs (Table 3B,C). The lower leg is retracted during the stance phase and reaches a horizontal orientation at lift-off (mean 1° at symmetrical gaits, 3° in trailing and 7° in leading limbs at in-phase gaits). In some species, the minimum angle of the lower leg is observed during the stance phase and afterwards the angle increases until lift-off by retraction of the foot at the end of stance. This biphasic motion of the shank (i.e. with two minima during one step cycle) is most pronounced in Tupaia at all gaits (Fig. 3A,3B,3C). Lower leg retraction reaches its maximum during the swing phase in all species at symmetrical gaits and in most species at in-phase gaits. Mean amplitudes are higher in all species at in-phase gaits than at symmetrical gaits, but are comparable in Monodelphis. Mean amplitudes of trailing and leading limbs are nearly the same in all species.
The foot is in matched motion with the thigh, seen in particular during the stance phase at all gaits (Fig. 3A,3B,3C). Mean touch-down angles of all species occur over a small range of 4-19° at all gaits. As the foot is brought down, it is in a semidigitigrad position in all species, with the most erected foot seen in Procavia. The foot is in retraction and crosses its vertical position in all species during the stance phase at all gaits. Mean lift-off angle is variable at different gaits, ranging between 92° and 138° (Dasyuroides and Tupaia) at symmetrical gaits, 78-121° in trailing limbs and 81-126° in leading limbs (Ochotona and Procavia) at in-phase gaits. Foot retraction is more restricted at in-phase gaits than at symmetrical gaits in all species (except Dasyuroides). After reaching its maximum retraction, the foot is protracted during the swing phase and the following retraction starts just before the next touch-down. Mean amplitudes of all species are highest at symmetrical gaits (104°), slightly lower in the leading limb (101°), and lowest in the trailing limb at in-phase gaits (99°).
Contribution of hindlimb segment movements to step length
Whereas the femur is the most propulsive segment at symmetrical gaits with
a mean contribution of 76% to step length in all species, `pelvic movements'
contribute to half of the step length at in-phase gaits
(Table 3A-C). At symmetrical
gaits, the contribution of `pelvic movements' is in the same low order as
amplitudes for all species ranging between -3% and 7%. The highest value was
found in Microcebus (10%). At in-phase gaits, the contribution of
`pelvic movement' to step length is similar in all species because the same
effective angular displacement of the pelvis occurs in species with and
without tails. Values are also comparable for trailing and leading limbs in
most species. The only differences observed were in Galea and
Ochotona, where the contribution of `pelvic movements' to trailing
limbs is higher than to the leading limbs in Galea and the reverse is
true for Ochotona (Table
3B,C). Displacement of the thigh at in-phase gaits contributes to
about one third of the step length, but these data are highly variable between
different species. The lowest values for contribution of thigh displacement to
body forward movement were found in Ochotona (which also showed the
lowest EAD) with only 8% in the trailing and 10% in the leading limbs. The
highest values of EAD, which resulted in higher contributions to step length,
were observed in Tupaia (46% in trailing limbs and 53% in leading
limbs). Comparable values were calculated for more distal segments for
hindlimbs at symmetrical gaits and for trailing and leading limbs at in-phase
gaits. In general, the foot contributes more to step length (18% at
symmetrical gaits and about 12% at in-phase gaits) than the shank (3% at
symmetrical gaits, 9% in trailing and 4% in leading limb at in-phase gaits).
The reverse case, in which the contribution of shank movements exceeds the
contribution of foot movements was found only for Ochotona and
Procavia at in-phase gaits and for Procavia and
Rattus at symmetrical gaits.
Kinematics of hindlimb joints
In general, flexion and extension of all hindlimb joints are more
pronounced during symmetrical gaits than during in-phase gaits (Fig.
3A,3B,3C).
Comparisons of the limb joint behaviour of all species at in-phase gaits point
to Ochotona as the species with the most restricted angular
excursions and to Tupaia as the species with most extensive angular
excursions. A biphasic angular movement, including one flexion and one
extension per each stance and each swing phase, was found for knee and ankle
joints in all species at all gaits. In contrast, hip joints show a monophasic
behaviour at symmetrical and in-phase gaits, meaning that extension enters
into a short plateau during the first 20% of stance at in-phase gaits (with
the exception of Tupaia). At symmetrical gaits, the extension of the
hip joint starts shortly before touch-down (80-95% of duration of the previous
step cycle). There, it lasts until 90% of the stance phase in
Microcebus and Tupaia, until 10% of the swing phase in
Monodelphis and until lift-off in all other species. At in-phase
gaits, extension reaches its maximum before lift-off of the
trailing limb of Procavia and Ochotona, at
lift-off in Dasyuroides and after lift-off in all other
species. Maximum angular extension of the hip joint in leading limbs occurs
after lift-off in all species, but ends at lift-off in Ochotona.
The knee flexes before touch-down in all species at all gaits and reaches its maximum flexion at mid-stance when the foot passes underneath the hip joint. Knee joint extension, however, starts at different times at the end of stance. Knee joint extension ends independently from gaits in only two species; at lift-off in Dasyuroides and after lift-off in Monodelphis. Knee joint flexion at symmetrical gaits starts before lift-off in Rattus and Microcebus and at lift-off in Tupaia, Galea, and Procavia. At in-phase gaits, extension ends at lift-off in trailing and leading limbs of Galea and after lift-off in Tupaia and Procavia. In Ochotona, knee joint flexion starts earlier in trailing than in leading limbs.
The stance phase extension of the ankle joint continues into the subsequent swing phase in all species at symmetrical gaits. In most of the species, no major changes in timing were observed during the change from symmetrical to in-phase gaits. In Ochotona, in which only in-phase gaits were analysed, flexion starts before lift-off in trailing and in leading limbs.
The highest CSP has the hip joint in all species indicating a high degree of horizontal versus vertical action (Table 3A-C). Values within species are higher at symmetrical gaits than at in-phase gaits. With a mean touch-down angle of 40° in all species, the hip joint is flexed more at symmetrical gaits than at in-phase gaits (56° in trailing and 50° in leading limbs). Whereas hip joint angles at touch-down are similar in trailing and leading limbs of Monodelphis and Dasyuroides, they are higher in the trailing than in the leading limbs in all other species.
The range of mean touch-down angles for all species at in-phase gaits is twice that of symmetrical gaits, but is higher at symmetrical gaits than at in-phase gaits for mean lift-off hip joint angle. The lowest mean value of the hip joint at lift-off was found in Dasyuroides (73-80°) and the highest value in Tupaia (110-141°) at all gaits. Mean (±S.D.; lift-off angles of all species under study are 111±21° at symmetrical gaits, 96±11° in the trailing limb and 100±11° in the leading limb at in-phase gaits. At lift-off, the hip joint of the leading limb is extended more than that of the trailing limb in Dasyuroides, Galea and Procavia and is nearly the same in both hindlimbs in the other species. Mean lift-off angle decreases with the change from symmetrical to in-phase gaits in most species, but is comparable between both gaits in Procavia and lower at symmetrical than at in-phase gaits in Dasyuroides. Owing to the higher values at touch-down and lower values at lift-off for in-phase gaits compared to symmetrical gaits, EAD is reduced at in-phase gaits. Mean maximum angular movement amounts to 75° at symmetrical gaits, to 45° in trailing limbs and to 54° in leading limbs at in-phase gaits in all species. The highest overall amplitudes were observed in Tupaia (110°) at symmetrical gaits and the lowest in the trailing limb of Ochotona at in-phase gaits (26°).
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Discussion |
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Observations on forelimb movement of the walking Didelphis
marsupialis (Jenkins and Weijs,
1979) correspond to those of our small mammals. In
Didelphis, scapular angle at touch-down ranges between 40-50° and
the humerus is oriented almost vertically. Shoulder and elbow joints are
extended approximately 130° and 110°. The touch-down position of the
forelimb in Cavia porcellus
(Rocha Barbosa et al., 1996
)
is very similar to that of its near relative Galea at all gaits. In
the case of exploratory walking in Rattus norvegicus
(Jenkins, 1974b
), overall
forelimb excursions are reduced and the point of touch-down lies slightly
ahead of a point directly beneath the shoulder joint. In this case scapular
touch-down angle is higher (50-60°) and humeral angle is smaller (45°)
in exploratory walking compared to moderate walking. Limb kinematics were
documented cineradiographically for a series of small mammals by Jenkins
(1971
). Differences in humeral
touch-down angles and positions of touch-down points between the species
studied by Jenkins and our sample of small mammals are probably caused by the
slow speed of the exploratory walk investigated by Jenkins.
In Felis catus f. domestica, the forelimb is more extended at
touch-down than in our animals. Whereas the scapular angle measured in
cineradiographic studies is the same as in our species (40-46°;
Boczek-Funcke et al., 1996),
shoulder and elbow joint angles are about 30° higher. Scapular touch-down
angles obtained in Felis (using externally applied markers) amount to
40-50° (Miller and Van der
Meché, 1975
; English,
1978a
,b
;
Halbertsma, 1983
). In
primates, forelimb posture at touch-down is characterised by an increasing
amount of extension in the shoulder and elbow joints, which together with
proportional changes between forelimb segments, results in a cranial
displacement of the touch-down point
(Jouffroy et al., 1983
;
Larson et al., 2000
;
Schmidt and Fischer, 2000
).
With increasing body size in arboreal-quadrupedal primates the forelimb
protraction augments (Schmidt and Voges,
2001
). Cineradiographic studies of shoulder movements in primates
indicate that the amount of scapular rotation is reduced in larger species by
both a higher touch-down angle (57° in Cercopithecus aethiops:
Whitehead and Larson, 1994
;
49° in Eulemur fulvus:
Schmidt and Fischer, 2000
) and
a lower lift-off angle. Only Capra hircus, the domestic goat,
deviates clearly from other mammals in having a more extended limb, with
shoulder joint angles of more than 135° and elbow joint angles of 120°
(Lilje and Fischer, 2001
).
Scapular retraction starts at an angle of 61° in Capra and
56° in Tragulus javanicus (the mouse deer; unpublished data)
(Fig. 5).
|
Whereas the forelimbs show no fundamental geometrical differences between
symmetrical gaits and in-phase gaits, in that three segments are always
displaced, hindlimb protraction is also executed by three hindlimb segments at
symmetrical gaits. At in-phase gaits, intervertebral lower spine movements
(causing a sagittal `pelvic displacement') act functionally as an additional
fourth segment. Despite this, femoral position is comparable at all gaits
being almost horizontal at touch-down (in all species = 7±10° at
symmetrical gaits, -2±5° in trailing limbs and -6±5° in
leading limbs at in-phase gaits; means ± S.D.). This position is
achieved by hip joint movement at symmetrical gaits, but is mainly passively
induced by sagittal spine flexion (and to a lesser degree to hip joint
flexion) at in-phase gaits. As occurs in the forelimb, the distal segment is
in matched motion with the femur. The foot is in the same position (S.D.
5°) 12° at symmetrical gaits, 10° in trailing limbs and 9°
in leading limbs at in-phase gaits. At symmetrical gaits, hip joints of all
species have relatively similar positions at touch-down, indicated by a
relative low value of S.D. (40±5°). The knee joint, however, shows
a little more variation (75±12°) and the ankle joint is the most
variable (80±20°). Standard deviations increase in hip joints
(56±12° in trailing limbs and 50±10° in leading limbs)
whereas they are nearly constant, or decrease, in knee joints
(77±11° resp. 75±6°) and ankle joints (89±16°
resp. 87±14°) at in-phase gaits.
Quantitative data on sagittal pelvic displacement are available for
Cavia at trot and gallop (Rocha
Barbosa et al., 1996). Its touch-down angle of 28° is similar
to Galea and the two metatherians at symmetrical gaits. The high
value of 70° at gallop corresponds to the data of tailless species in our
sample. Gasc (1993
) described
hindlimb kinematics in the tailed rodent Meriones shawi at gallop.
Although pelvic displacement was not quantified, angles at touch-down and
lift-off can be estimated from a stick-figure drawing. Touch-down angles in
Meriones are approximately 34° for trailing linbs and 32° for
leading limbs and are always smaller than values measured in our tailed
species. The pelvis touch-down angle of the walking Mephitis mephitis
was also estimated from a stick-figure drawing (45°;
Van de Graaff et al., 1982
)
and lies in the range of our observations.
Descriptions of hindlimb movements are available for a series of small to
medium sized mammals. The touch-down position of the thigh in Didelphis,
Tupaia, Mustela putoris (ferret), Mesocricetus auratus
(hamster), Heterohyrax brucei (hyrax), and Rattus is more or
less horizontal (Jenkins,
1971), and corresponds to angles reported here. The same is true
for the Cavia (Rocha Barbosa et
al., 1996
) and for both trailing and leading limbs in the
galloping Meriones (Gasc,
1993
). As observed by Jenkins and Camazine
(1977
), the thigh is
protracted at an angle of 30° below the horizontal line in Felis,
Vulpes fulva (the fox) and Procyon lotor (the racoon) at
touch-down. The highest mean touch-down angle of the thigh (51°) is given
for Mephitis by Van de Graaff et al.
(1982
). The more retracted
thigh in Felis (Kuhtz-Buschbeck
et al., 1994
) and Mephitis reflects a more extended limb
with higher extension of both hip joint (65° and 97°, respectively, in
comparison to our sample mean 43°) and knee joint (120° and
154-73°). The ankle joint angles are also more extended, being
approximately 30° in Felis
(Kuhtz-Buschbeck et al., 1994
)
and 60° in Mephitis (Van de
Graaff et al., 1982
).
Limb configuration at lift-off
Limb configuration of the forelimb at lift-off consists of a vertically
placed scapula (in all species 92±7° at symmetrical gaits,
87±9° at in-phase; means ± S.D.) and a nearly horizontally
placed humerus, especially at in-phase gaits (-13±7° respectively
-2±9°). The scapula initiates lift-off
(Roberts, 1974), more or less
waiting the last 20 % of the stance phase for the other joints to take off.
The actual lifting off is caused by a strong flexion in the elbow. It is
interesting to note that elbow extension decreases with increasing speed at
walk and slow trot but increases with increasing speed at in-phase gaits
(Fischer, 1998
;
Fischer and Lehmann, 1998
;
Schilling and Fischer, 1999
;
Schmidt and Fischer,
2000
).
The mean (±S.D.) lift-off angle of the pelvis (30±11°) compared to that at touch-down (33±11°) indicates that only minor `pelvic movements' occur at symmetrical gaits. Lower mean values for pelvic lift-off position, in the leading compared to trailing limbs, is caused by the ongoing sagittal extension during stance (18±18° versus 21±18°). In comparison to limb configuration at touch-down, hindlimb position at lift-off is more variable among all species, especially in the knee joint, caused by differences in retraction excursions of the thigh. Knee joint and thigh lift-off position are more variable between all species at symmetrical gaits (83±27°, 81±26°) than in trailing limbs (78±23°, 75±23°) and leading limbs (87±17°, 82±22°) at in-phase gaits. Hindlimb configuration at lift-off is marked by a horizontal positioning of the shank at all gaits (in all species = 1±11° at symmetrical gaits, 3±16° in trailing limbs and 7±14° in leading limbs at in-phase gaits; means ± S.D.).
The pelvis in Mephitis is in a more inclined position at
touch-down and at lift-off at symmetrical gaits (38°;
Van de Graaff et al., 1982)
indicating a more inclined position in general in comparison to data presented
here (30°). Effective angular movement of the pelvis is a little bit
higher in Cavia (12°; Rocha
Barbosa et al., 1996
) than in Galea (3°), but the
amplitude (10°) is comparable. The more extended limb configuration in
Felis and Mephitis at symmetrical gaits is also represented
in lift-off positions of hindlimb joints. At mean lift-off angles in hip and
knee joints of 130° in Felis
(Kuhtz-Buschbeck et al., 1994
)
and of 163° and 149°, respectively, in Mephitis
(Van de Graaff et al., 1982
),
all of these values are clearly higher than those of the species we studied
(111°, 83°). Ankle joint angles at lift-off augment with increasing
speed in Felis (113-146°;
Kuhtz-Buschbeck et al., 1994
)
and are comparable at lower speeds (0.33-1.19 m s-1) to the mean
angle we observed (115°). In comparison, the ankle joint is more flexed at
lift-off in Mephitis (i.e. 84° at 0.28 m s-1;
Van de Graaff et al.,
1982
).
At in-phase gaits, femoral retraction of the trailing limb in the species
studied here (47-109°) range between values for Meriones
(60°; Gasc, 1993) and
Cavia (90°; Rocha Barbosa et
al., 1996
). Values for Galea (mean 86°) investigated
here are comparable to those for Cavia (90°;
Rocha Barbosa et al., 1996
)
indicating a nearly vertical position. Overall, the more inclined pelvic
position in Cavia at in-phase gaits
(Rocha Barbosa et al., 1996
),
indicates that pelvic positioning is similar to other tailless species studied
here, except Galea. However, amplitudes and effective angular
movements are comparable between both caviids. As in our tailed species, the
pelvis is also oriented very near to the horizontal at lift-off in
Meriones (6° for trailing and 9° for leading limbs;
Gasc, 1993
). The hip joint in
the trailing limb is flexed most at lift-off in Meriones (65°,
Gasc; 1993
), extended a little
bit more in the species included in our study (mean 96°, range
93-112°) and extended most in Cavia (115°;
Rocha Barbosa et al., 1996
).
As in the hip joint, the knee joint is also flexed more in Meriones
(51°; Gasc, 1993
) than in
our species (59-119°) or in Cavia (100°;
Rocha Barbosa et al., 1996
).
As far as the ankle joint is concerned, values for both Meriones
(119°; Gasc, 1993
) and
Cavia (107°; Rocha Barbosa et
al., 1996
) are well within the range of values reported here
(91° to 125°).
Amplitudes during stance phase
Differences between symmetrical and in-phase gaits, observed in all joints,
point to more elevated limbs in the latter gaits
(Fig. 5, Tables
2A,B,
3A-C). As the extended position
is held throughout the stance and flexion reduced, especially at midstance,
all amplitudes of limb joints decrease during the transition from symmetrical
to in-phase gaits in all species we studied.
Scapular amplitudes range between 44° (Dasyuroides) and
60° (Galea and Rattus) during the stance phase at
symmetrical gaits. These amplitudes are reduced at in-phase gaits, ranging
from 37° to 48°. Previously published values on scapular rotation in
walking Rattus collected from cineradiography are lower than those
measured here by approximately 15°
(Jenkins, 1974b, but see our
earlier remarks on slow exploratory walk). In Didelphis, scapular
rotation amounts to 40° at a slow walk or to 50° at a fast walk
Jenkins and Weijs, 1979
). The
amplitudes of scapular rotation in Cavia deviate from those of our
species by having higher values at both symmetrical (trot: 62°) and
in-phase gaits (gallop: 70°), caused mainly by an extraordinary high angle
at lift-off (107-115°). Scapular amplitudes range from 38° (walk) to
42° (trot and gallop) in Felis
(English, 1978b
). Whereas the
values for the walking Felis have been confirmed by a later
cineradiographic study (40°; see
Boczek-Funcke et al., 1996
),
scapular rotation is underestimated in trotting Felis (58°;
Sontag and Cremer, 1978), most probably due to the external registration
techniques of English's study.
Published data on shoulder joint amplitudes are in accordance with our
observations. While maximum amplitudes during stance are relatively low in
Felis (24-28°; Boczek-Funcke
et al., 1996), observations in Didelphis (35-45°;
Jenkins and Weijs, 1979
) and
Cavia (46° at symmetrical and 35° at in-phase gaits;
Rocha Barbosa et al., 1996
)
are close to ours. The amplitudes of elbow joint excursions during the stance
phase in Felis (41°), Didelphis (40°) and
Cavia (42°) at symmetrical gaits, lie within the same small range
as in the species analysed in this study. The digitigrad Felis
resembles the digitigrad Procavia in overall behaviour of the wrist
joint (Caliebe et al., 1991
;
Miller and Van der Meché,
1975
) inasmuch as amplitudes are relatively low, especially with
increasing speed and dorsiflexion is restricted.
Amplitudes of `pelvic movements' are highly comparable between all species
under study indicated by low standard deviations at symmetrical (3°) and
at in-phase gaits (8° in trailing and 5° in leading limbs). The mean
amplitude of `pelvic movements' for all species in the current study is
12° at symmetrical gaits, the same as reported for Cavia
(Rocha Barbosa et al., 1996).
At in-phase gaits, the mean amplitudes of `pelvic movements' range between
27° and 49° in trailing limbs and between 31° and 46° in
leading limbs. The value for the trailing limb in Cavia is within the
range given here (48°; Rocha Barbosa
et al., 1996
) and is only a little bit higher than the mean value
observed for Galea (44°). The amplitude of thigh movements in the
species studied here (during the stance phase at symmetrical gaits) ranges
between 51° (Dasyuroides) and 84° (Monodelphis) in
most species and is higher only in Tupaia (110°). Values given by
Jenkins and Camazine (1977
)
for Vulpes, Mephitis and Felis (63°, 72° and 72°
respectively) are in-between the range we observed. For in-phase gaits, data
for femoral amplitudes at stance phase are only available for the trailing
limb in Cavia (48°; Rocha
Barbosa et al., 1996
) and for the leading limb in
Meriones (70°; Gasc,
1993
). These values are comparable to those reported here, which
range between 50° (Ochotona) and 98° (Monodelphis)
in the trailing limbs and between 61° (Ochotona) and 109°
(Tupaia) in the leading limbs. Whereas mean hip joint and knee joint
amplitudes are comparable to each other at in-phase gaits (45° and 43°
in trailing limbs and 54° and 44° in leading limbs), hip joint
amplitude in the current study is twice as high as knee joint amplitude at
symmetrical gaits (75° and 38° respectively). Hip and knee joint
amplitudes are clearly different at all gaits in Cavia being 63°
and 25° at trot and 63° and 35° in the trailing limb at inphase
gaits (Rocha Barbosa et al.,
1996
). A remarkable decrease in the mean amplitude occurs in the
ankle joint of Cavia during the change from symmetrical (80°) to
in-phase gaits (17° in trailing limb)
(Rocha Barbosa et al., 1996
).
The mean amplitude of the trailing limb in Cavia falls short of the
range observed here (35° in Ochotona and 74° in
Monodelphis), but the value for ankle joint amplitude at symmetrical
gaits is in between the range we found (36° in Microcebus and
88° in Tupaia).
To summarize, kinematics accompanying the transition from symmetrical to
in-phase gaits offer no uniform pattern as implied by earlier studies, which
discussed reduced joint amplitudes at in-phase gaits compared to symmetrical
gaits. Studies of the majority of limb joints in Procavia
(Fischer, 1994) or of the
shoulder joint in Cavia (Rocha
Barbosa et al., 1996
) suggested that angular movements at in-phase
gaits were reduced, but there is no species-independent, single pattern that
accompanies the transition from symmetrical to in-phase gaits. In the case of
scapular movements and hip joint angular movements, amplitudes decreased in
all of our species at in-phase gaits. In Cavia, however, scapular
displacements increased and hip joint angular movements remained constant
(Rocha Barbosa et al., 1996
).
Whereas amplitudes decrease during the change from symmetrical to in-phase
gaits in the shoulder joints of Procavia, Monodelphis, and
Cavia (Rocha Barbosa et al.,
1996
), they increase in Galea and remain constant in
Dasyuroides and Tupaia. Elbow joint excursions increase at
in-phase gaits in Monodelphis and Galea and decrease in all
other species. Wrist joint angular movements are more pronounced at
symmetrical gaits than at in-phase gaits in Monodelphis, Dasyuroides
and Tupaia. The reverse is true for Procavia, Galea, and
Cavia (Rocha Barbosa et al.,
1996
). In the hindlimb, knee joint amplitudes decrease at inphase
gaits only in Tupaia and increase in all other species, including
Cavia (Rocha Barbosa et al.,
1996
), but are constant in Galea. Ankle joint amplitudes
at in-phase gaits are only one quarter as high as at symmetrical gaits in
Cavia (Rocha Barbosa et al.,
1996
). Although not as dramatic as in Cavia, decreases
are also observed for ankle joint amplitudes in Galea and
Tupaia, while increases were observed in all of the species we
studied.
Contribution of segments to step length
The `overlay method' approach (Fischer
and Lehmann, 1998) that we used to calculate the contribution of
displacements of different segments to step length, explicitly considers the
vertical displacement of pivots during stance. As this is the first study that
compares the segment's contribution to step length, no other data outside our
working group are available for comparison. Calculations indicate the
predominance of scapular retraction in forelimb movement, while the
contribution of humeral displacement to step length is always less than half
of the scapular value. The contribution of the forearms only exceeds the value
of the upper arm in species in which the forearm is extensively retracted,
such as Tupaia at symmetrical gaits or Galea at in-phase
gaits. Hand movements contribute to step length in most species with
approximately 5 % and never more than 10 %.
Despite the different limb configuration of artiodactyls and the lowest
amplitudes of scapular rotation observed, the contribution to step length of
the most proximal segment is the highest (73%) in the goat, simply because of
the high scapular pivot (Lilje and
Fischer, 2001). Our calculations of the scapular contribution does
not consider translation of the scapula along the thoracic wall known from the
aclavicular Felis (Boczek-Funcke
et al., 1996
) and Procavia
(Fischer, 1998
). The more
extended limbs observed in most species at in-phase gaits lead to a more
elevated position of the body and thus a higher scapular or elbow pivot. So
the same or even higher contribution to step length can be achieved by lower
effective angular movements (EADs).
As in the forelimb, analysis of the contribution of segment's movement to step length, point to the most proximal element as the most propulsive segment in the hindlimb. Because of the fundamental change in hindlimb motion between symmetrical and in-phase gaits, resulting in a different number of acting segments, distinct changes in the contributions of individual hindlimb segments occur. At symmetrical gaits, femoral protraction and retraction contribute three-quarters to step length and the remainder is mainly contributed by foot and shank movements. `Pelvic movements' contribute only to a lesser degree. In contrast to this, the main part of body propulsion half the step length is contributed by additive sagittal spine movements at in-phase gaits. Despite the differences in touch-down and lift-off positions of the pelvis in tailed and tailless species, their contribution of `pelvic movements' is comparable, owing to similar effective angular movements. One third of step length is added by thigh movement at in-phase gaits and the rest is shared by foot and shank movements.
Final conclusion
The comparison of kinematic data of different therian mammals suggests that
therian mammals with small body sizes (90-2500 g) display the same overall
behaviour of limb displacement during locomotion. To test this hypothesis, we
included Procavia in our analysis, which descends most probably from
larger cursorial ancestors and is secondarily dwarfed
(Thenius, 1979; Fischer,
1986
,
1992
). Tragulus, the
smallest ruminant, also supports the hypothesis that mainly body size
constraints the kinematic pattern (Fig.
5).
In general, kinematics of small therian mammals are obviously independent of their systematic position (at least in species selected here), of their natural habitat (when we accept that kinematics on the treadmill parallels unrestrained kinematics), and also of specific anatomical dispositions. Obviously, characters such as finger or toe reduction, fusion of zygpopodial elements, reduction of the clavicle, carpal or tarsal specializations, and even extreme elongation of metapodials in Tragulus do not affect the overall kinematic pattern of therians.
The consequences of gait change from symmetrical to in-phase gaits are
strikingly different on forelimb and hindlimb. Whereas only timing changes on
the forelimb (kinematics remain the same!), hindlimb kinematics change
significantly. In small therian mammals, in-phase gaits are marked by an
extensive sagittal bending of the lumbar spine as has been shown by
cineradiography. Small intervertebral movements add up and pelvic retro- and
protraction is their obvious effect
(Fischer, 1994;
Rocha Barbosa et al., 1996
;
Schilling and Fischer, 1999
).
Sagittal spine movements contribute roughly one half to the total propulsive
movement during stance at inphase gaits. The occurrence or absence of a long
tail influences the pelvic position at touch-down and lift-off but not the
total displacement. The pelvic course of movement starts from a nearly
vertical position in tailless species and at a more caudally inclined position
in tailed species. It ends at a horizontal position in tailed species at
lift-off and a more inclined position in tailless species
(Fig. 4). We have problems
interpreting the graph of the tailless Galea since it behaves more
like a tailed species. For example, observations on Cavia
(Rocha Barbosa et al., 1996
),
a sister taxon of Galea, show the typical pelvic course of movements
as in our tailless species.
Studies on midsize carnivores (Felis, Vulpes, Procyon) and our data on Capra strongly suggest that the elevated limb position of these forms has some influence on their kinematics. Still, the three-segmented fore- and hindlimbs are displaced in the same proximal pivots as in the smaller therians, and these are situated at the same level. While the scapular displacement remains the same in Felis, scapular EAD is reduced in Capra. In contrast, the high location of the scapular pivot leads to the highest contribution to step length in this artiodactyle. As a consequence of the more extended limbs, the position of humerus, femur and shank is more inclined at the beginning and end of stance with respect to their horizontal position in small therians. As there are no cineradiographic data on midsize or even larger mammals at in-phase gaits, we cannot estimate the impact of gait change on kinematics and especially on lower spine movements.
The identification of a basically uniform pattern of kinematics in small
therians leads to the suggestion, that mesozoic mammals of the therian stem
lineage, which have been small to very small
(Jenkins and Schaff, 1988;
Krebs, 1991
;
Hu et al., 1997
;
Ji et al., 1999
;
Luo et al., 2001
) had the same
kinematic pattern. This configuration of limb segments is considered to
represent the ancestral therian design of limbs with respect to other amniotes
and especially monotremes (Pridmore,
1985
). Its main function can be seen as an adaptation to
irregularities of the ground. Such irregularities are thought to pose major
handicaps for therians with parasagittal placed limbs
(Fischer, 2001
). Relative to
small body sizes, support on ground or on off-ground strata are comparable, as
has already been pointed out for Tupaia by Jenkins
(1974a
). Therefore, discussion
on arboreality in small mammals seems inadequate.
In summary, basic elements of locomotion of small to midsize therians are: (1) a three-segmented limb with zigzag configuration, which is mainly displaced at the highest possible pivot; (2) position of scapular pivot and hip joint at the same height over the ground at symmetrical gaits and consecutively similar functional length of fore- and hindlimbs; the matched motion of two segments (scapula/lower arm, femur/metatarsus) during retraction of limbs; (3) kinematics of forelimbs are independent of speed and gait; (4) the fundamental change from femur retraction at symmetrical gaits to sagittal spine movement at in-phase gaits resulting in different hindlimb kinematics; (5) propulsive movement of the body is mainly achieved by the most proximal acting limb segments (scapula and femur at symmetrical gaits, scapula and sagittal spine movements at inphase gaits) while all further distal limb joints contribute only to a lesser degree to step length.
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