Biomechanics and kinematics of limb-based locomotion in lizards: review, synthesis and prospectus

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Ž.
Comparative Biochemistry and Physiology Part A 131 2001 89￿112
Review
Biomechanics and kinematics of limb-based locomotion
in lizards:review,synthesis and prospectus
￿
A.P.Russell
a,
￿
,V.Bels
b
a
Vertebrate Morphology Research Group,Department of Biological Sciences,Uni
￿
ersity of Calgary,2500 Uni
￿
ersity Dri
￿
e N.W.
Calgary,Alberta,Canada T2N 1N4
b
Centre Agonomique de Recherches Appliquees du Hainaut,rue de l’Agriculture 301,B-7800 Ath,Belgium
´
Received 13 January 2001;received in revised form9 May 2001;accepted 11 May 2001
Abstract
The sprawling pattern of locomotion in lizards is kinematically intriguing and is underpinned by a distinctive pattern
of appendicular morphology.The statics of the sprawling posture dictate fundamental design principles,and these place
constraints on the three-dimensional kinematics of the limbs and body axis as locomotion is effected.The fore and hind
limbs accommodate these constraints and dictates in fundamentally similar,but positionally different ways,resulting in
different kinematic profiles for these two appendages.Recent kinematic investigations have helped to clarify earlier
generalizations about lizard locomotion and have revealed that kinematic patterns are more variable than was
previously supposed.Such analyses,and attendant detailed studies of the anatomy of the locomotor system,promise a
new synthesis and enhanced understanding of evolutionary patterns of locomotion of lizards and adjustment to various
locomotor substrata and modes of progression.￿ 2001 Elsevier Science Inc.All rights reserved.
Keywords:Lizards;Locomotion;Kinematics;Gait;Quadrupedalism;Bipedalism;Anatomy;Arthrology;Ecomorphology
1.Introduction
Unlike the case with cranial features and feed-
ing morphology and mechanisms,the employment
of locomotor structures as a source of systematic
features has not been widespread.Except for the
Ž.
contribution of Sukhanov 1961,locomotor mor-
phology has played a relatively minor role in
systematic studies of lizards.Beyond the purely
￿
This paper was originally presented as part of the ESCPB
Congress symposium ‘Learning about the Comparative
Biomechanics of Locomotion and Feeding’,Liege July 26￿27,
`
2000.
￿
Corresponding author.Tel.:￿1-403-220-5198;fax:￿1-
403-289-9311.
Ž.
E-mail address:arussell@ucalgary.ca A.P.Russell.
descriptive,however,investigation of the locomo-
tor system has been spurred by the desire to more
fully comprehend how form and function are re-
lated in the context of locomotor behavior and
kinematics.Such investigations have either at-
tempted to deduce these relationships by extrap-
olating from anatomy to potential function,or
have employed some form of kinematic analysis
to relate behavior to gross morphology.
Anatomical knowledge and kinematic analyti-
cal techniques are now both sufficiently devel-
oped that they can become reciprocally illuminat-
ing,although little in the way of this synthesis has
so far occurred.The following review outlines
what has so far been learned about locomotion in
lizards and provides both a context for a synthesis
of this information and the suggestion of future
1095-6433￿01￿$ - see front matter ￿ 2001 Elsevier Science Inc.All rights reserved.
Ž.
PII:S 1 0 9 5 - 6 4 3 3 0 1 0 0 4 6 9 - X
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿11290
directions.It also provides the opportunity to
indicate how anatomy may be more effectively
employed to understand locomotor behavioral
differences and convergences within and between
clades of lizards.
2.Sprawling posture
Two fundamental types of limb posture and
associated gait are recognized in tetrapods
Ž
Ostrom,1969;Bakker,1971;Charig,1972;Rew-
.
castle,1981,1983.That found in salamanders
and lizards is termed ‘sprawling’,with the body
Ž.
slung between laterally projecting limbs Fig.1.
Kinematically,this results in a three-dimensional
approach to locomotion,with limb segments mov-
ing in different planes in space and,in some
Ž
instances,with different senses of motion Rew-
.
castle,1981,1983;Landsmeer,1984.Posture in
mammals,dinosaurs and birds,is termed ‘erect’,
the limbs being held under the body and their
movement restricted to a vertical,parasagittal
plane,and is,therefore,kinematically two-dimen-
sional,with all limb segments moving essentially
Ž.
in a single plane Rewcastle,1981.
The characterization of sprawling type limb
posture as one in which the limbs project laterally
Ž.
from the body at least while the body is at rest,
with limb movement being confined to an essen-
tially horizontal plane,is a considerable oversim-
plification.Limb movement in the sprawling gait
is complex and limb posture changes considerably
Ž.
during the limb stroke see below.The single
essential criterion of the sprawling gait is that the
humerus and femur cannot attain an orientation
with their long axes vertically directed.Thus,
rather than moving in a fore and aft sense,the
humerus and femur move backwards,outwards
Ž.
and downwards during the retraction stance
stroke.Such movements complicate the operation
of the distal limb segments and dictate their rela-
tive effectiveness as active participants in the
production of locomotor thrust.
A number of authors have considered sprawl-
ing to be a ‘primitive’ mode of progression.Charig
Ž.
1972,for example,discussed the ‘improvement’
of gait towards the erect condition.Although the
sprawling habit of locomotion was evidently that
of the earliest tetrapods,lizards,while retaining
this basic mode,also demonstrate a variety of
specializations peculiar to themselves,and it is
more appropriate to regard sprawling and erect
modes of locomotion as fundamentally different
Ž.
types Rewcastle,1981.
Ž.
Rewcastle 1981 saw the sprawling stance as
being adaptive for small tetrapods because of its
inherent stability and postulated that it may be of
special value in climbing.Its advantages for small
animals that rely primarily on sprinting,frequent
Ž
acceleration intermittent locomotion may be of
.
significance in this regard and the ability to move
on varying,and often inclined,substrates,was
Ž.
considered by Christian 1995.In large tetrapods
body support in this mode becomes problematic,
and for cursors it is not particularly effective,as
vertical displacements of the center of mass are
not produced by limbs moving in a near-horizon-
tal plane.Thus,the suspended phase in sprawlers
is either extremely short or absent,and the gallop
is unattainable unless dorsoventral vertebral
Ž
bending is introduced as in crocodilians,Zug,
.
1974;Webb and Gans,1982.Bipedalism during
rapid locomotion in lizards overcomes these in-
herent ‘problems’ and permits greater cursorial
ability by permitting a long suspended phase,thus
Ž.
increasing stride length Irschick and Jayne,1999
Ž.
but not necessarily speed.Bipedalism see below
results from the outcome of differentially propor-
tioned fore and hind limbs associated with rapid
acceleration in sprawlers,and the reduction of
Ž
interference between fore and hind limbs Chris-
.
tian et al.,1994a.At increasingly higher speeds
the longer hindlimbs increasingly interfere with
the shorter forelimbs.Beyond a critical speed the
forelimbs cease to support the body,and support
and balance are transferred to the hindlimbs
Ž.
Christian et al.,1994a,b as the forelimb pendula
can no longer keep pace with the movement
patterns of the hindlimbs.In this manner the
constraints of the sprawling posture are partially
Ž.
escaped Santi,1990;Christian et al.,1994a,b,
but the architecture of the hip,knee and ankle
still dictate the basic trajectory of the hindlimb,
which never becomes erect in the mammalian
sense.
3.Statics of sprawling posture
The basic principles of the statics of sprawling
Ž.
posture were outlined by Gray 1944.In this
stance the limbs contribute towards body support
by acting in the combined capacity of struts and
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A.P.Russell,V.Bels ￿Comparati
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Fig.1.Diagrammatic representation of the statics of sprawl-
ing posture.The limbs act as transverse struts.The axes at a-t
and b-s are equally inclined to the vertical and both are
Ž.
assumed to be equally loaded W.As struts,they exert
against the glenoid cavities inwardly directed horizontal forces
Ž
Wtan￿.As long as the lines of action of the forces R ￿
.
reaction of the ground operating at the feet pass through the
Ž.
centre of rotation of the glenoids and meet at a point X
Ž.
vertically above the centre of gravity G,the limbs can
Ž.
function as struts.The weight of the body 2W is transferred
Ž.
to the scapulae by the serratus muscles ser,and the force
exerted on the limb at each glenoid represents the result of
Ž.
the serratus tension S and the force exerted by the ventral
Ž.Ž.
elements of the girdle T.Modified after Gray,1944.
Ž.
levers Fig.1.The antebrachium and crus poten-
tially act as struts,forces being exerted along
their mechanical axes only.The humerus and
thigh potentially operate as levers and exert,
against the body and the ground,forces at angles
to their mechanical axes.Due to the slight incli-
nation at which the humerus and femur are held,
the limbs behave as inclined struts.
Problems of leverage are increased in rapid
forms as the humerus and femur must be long if
stride length,and hence speed,are to be in-
creased.The longer the propodials,the greater
the retraction arc of their distal ends,and the
Ž
greater the velocity of limb retraction Rewcastle,
.
1983;but at the same time,the lever arms on
which the body mass operates are longer,leading
to increased chance of collapse at knee and elbow
Ž.
Fig.1.This,to some extent,may be correlated
with change in propodial orientation as speed
Ž.
increases see below.
When a limb is acting as an inclined strut,the
couple exerted on it by the weight of the body
must be compensated by a couple due to a hori-
zontal force exerted on its end by the body,and
Ž.
friction or other horizontal force acting at the
foot.The horizontal force acting on the proximal
end of the limb represents the resultant horizon-
tal force exerted on the body by the other three
limbs.
In the sprawling posture typical of lizards a
large number of curvilinear muscles traverse each
joint and are able to stabilize these.Complete
stabilization of separate joints by means of one
long muscle is possible if the loading geometry of
all these joints is the same.For any other in-
Ž
stances,one or more short muscles one joint
.
muscles must be operative.
As a propulsive mechanism,the limb of a tetra-
pod functions as an extensible strut and as a
lever.In so far as it acts as a propulsive strut,the
limb is operated by its own intrinsic musculature.
In its function as a lever it is operated by its
‘extrinsic’ musculature,the distal end remaining
fixed at this time.
The diagonal coordination of limb movements
seen in lizards enables the limbs to propel the
body forward with a minimum of uncompensated
Ž
pitching or rolling couples Walker,1972;Grill-
.
ner,1975.The body is in static equilibrium with
its own weight at all phases of the quadrupedal
movement cycle,and can come to rest at any
point without toppling over.
4.Basic features of the propulsive stroke
Until recently little was known of the kinemat-
ics of lizard locomotion,and statements about
movement of limb segments were largely deduced
from extrapolations drawn from the manipulation
of skeletal preparations and living and freshly-
killed specimens,with occasional data being added
from cinematographic sources.
Ž.
Bakker 1971 discussed the major features of
the propulsive stroke of the forelimb of sprawlers
and divided it into five phases:humeral back-
swing;humeral long axis rotation;forearm rota-
tion;forearmflexion;and forearmextension.Such
components and their anatomical correlates have
been considered for various taxa by Landsmeer
Ž.Ž.
1980,1983,1984,Padian and Olsen 1984.
In association with the complexities of main-
taining contact of the manus with the substrate
during the propulsive phase of locomotion,com-
plex linked and integrated movements occur at
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A.P.Russell,V.Bels ￿Comparati
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Fig.2.Integration of movements at the shoulder,elbow and wrist that permit maintenance of manual contact with the substratum
Ž.Ž.
during the stance phase of the lizard forelimb.A-F,six stages in the stance phase in 1 lateral and 2 dorsal views.The elbow joint
Ž.
transmits humeral motion to the forearm ￿ the backward sway of the humerus solid arrows is translated into rotation of the
Ž.Ž.Ž.
antebrachium open arrows.The bicondylar distal articulatory facet of the humerus imposes rotation on the radius r and ulna u in
Ž.
the same direction open arrows.This necessitates specific adaptations of the antebrachial￿carpal articulations.The ulna-ulnare-pisi-
Ž.Ž.Ž.
form joint w1 is concentric,but the radius-radiale joint w2 is eccentric.G,the radioulnar ligament system lig combines these two
joints into a functional unit.I,in external rotation of the forearm,during the stance phase,the ligament is tightened.Once this has
occurred,further rotation of the forearm brings the radius and ulna closer together and axial rotation of the digital rays occurs.H,in
Ž.Ž.
the swing phase,the pronator profundus pron.prof.muscle relaxes the ligament system.Modified after Landsmeer,1983,1984.
Ž.
the shoulder,elbow and wrist joints Fig.2.The
humerus moves in the dorsoventral and antero-
posterior planes,as well as rotating about its long
axis;the antebrachial elements move in the an-
teroposterior plane while describing an arc with
respect to the proximal end of the humerus,and
rotate about each other;and the elements of the
wrist become realigned as the antebrachial ele-
Ž
ments move over the fixed manus Guibe,1970;
´
.
Landsmeer,1980,1983,1984.The anatomy of
the forelimb elements and the geometry of the
joints are reflective of this.
As a result of these integrated movements,the
forearm and manus move in a parasagittal plane
and the manus maintains firm contact with the
substratum,suffering little rotational slippage
Ž.
Padian and Olsen,1984.Overall,stride length
depends upon the integration of a number of
movements ￿ lateral undulation of the sternum
and thorax,translocation of the coracoid on the
sternum,anteroposterior excursion and axial ro-
tation of the humerus,and various movements of
Ž.
the forearm and manus Gans et al.,1997.Such
movements and their integration have been most
thoroughly documented for the shoulder region
Ž.
of Varanus exanthematicus Jenkins et al.,1983
Ž
and the wrist of Varanus sp.Landsmeer,1983,
.
1984.Pectoral girdle rotation contributes approx-
imately 30% of the forelimb stride in Lacerta,
Ž.
Dipsosaurus and Agama Peterson,1973.
Ž.
Bakker 1971 noted that in Permo-Carbonifer-
ous amphibians and early stem reptiles humeral
Ž.
torsion see below was much greater than it is in
living lizards,and that in these early forms the
long axis of the glenoid was nearly horizontal.
Despite these differences in geometry of the
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112 93
glenoid,humeral torsion and the associated
placement of the deltopectoral crest,Bakker
Ž.
1971 stated that these early forms already had a
typical sprawling pattern and that shoulder me-
chanics did not differ greatly from that of sala-
manders and Sphenodon.The major trend that
Ž.
Bakker 1971 identified in the transition to re-
cent saurians was not concerned with the me-
chanical configuration of the joints but with the
range of limb length to body weight ratios.In
early tetrapods this was much lower than it is in
Ž
living lizards,the shaft of the humerus and fe-
.
mur being much shorter and stouter than is
typical of living forms.
Humeral depression beyond 20￿ is not uncom-
mon in lizards,but is generally only possible when
the humeral long axis is perpendicular to the long
axis of the body,and such a position cannot be
maintained during humeral retraction as the dor-
sal lip of the glenoid cannot buttress the humeral
head.Thus,the humerus may be depressed dur-
ing static threat postures,intraspecific displays
and thermoregulatory posturing in geckos
Ž
Werner,1915;Brain,1958;Bustard,1967;
.
Werner and Broza,1969;Haacke,1976 and in
the typical head-bobbing intraspecific displays
Ž
seen in a variety of iguanids Carpenter,1961,
.
1962,1963.Some geckos,however,are able to
Fig.3.Integration of movements at the hip,knee and mesotarsal joints that permit maintenance of pedal contact with the substratum
during the stance phase of the lizard hindlimb.A,fully extended hindlimb in ventral view showing the elements and axes:fem,femur;
fib,fibula;tib,tibia;ac,astragalocalcaneum;1,5,first and fifth digits;lla,limb long axis;and kja,knee joint axis.B,depiction of the
orientation of the hinge-like knee joint axis with the femur flexed at 90￿ on the crus.The lateral side of the joint has its contact
Ž.Ž.Ž.
between the lateral condyle lat.cond.of the femur,the cyamella c and the meniscus m represented with bold lines.This pattern of
planar contact prevents long axis rotation at the knee and restricts the knee to a hinge-like action.C,the relationship of the vertical
Ž.Ž.Ž.
plane of the lateral surface of the lateral femoral condyle vert.plane lat.cond.to the knee joint axis kja and femoral long axis fla.
Ž.Ž.
D,geometry of the mesotarsal ankle joint.Astragalocalcaneum ac and fourth distal tarsal dt4 in dorsal view.The contours marked
Ž.
on the astragalocalcaneum,and body and ventral peg vp of the fourth distal tarsal indicate the sense of motion between the joint
surfaces.Axes 1 and 2 are the axes of primary curvature of the control surfaces of the two elements.These axes are structured like
Ž.
screw threads x,y and result in concomitant flexion-extension and rotation of the mesotarsal joint.E.Plantar flexion of the pes
Ž.
towards the end of the stance phase.The fifth digit 5 has lost contact with the substratum and the foot is rolling onto its mesial
Ž.
border,as indicated by the first digit 1:mt5,fifth metatarsal.F,diagrammatic representation of the kinematics of horizontal femoral
retraction and the resultant movements at the knee and mesotarsal joints.psp:parasagittal plane.Arrow indicates direction of travel.
Ž.
A,B,C,D modified after Rewcastle,1980;E modified after Brinkman,1980;F modified after Rewcastle,1981.
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A.P.Russell,V.Bels ￿Comparati
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walk for considerable distances with the limbs
Ž
held in a semi-erect posture Werner and Broza,
.
1969 and members of the genus Stenodactylus
may have glenoid and limb skeleton structure that
Ž
have converged on those of chamaeleons Gasc,
.
1963;Peterson,1973 ￿ investigation of the loco-
motor morphology and kinematics of Stenodacty-
lus could prove informative.
The gross movements of the hindlimb are simi-
Ž.
lar to those of the forelimb Bakker,1971,with
the long axis of the femur being depressed no
more than 20￿30￿ below the horizontal.The arc
of swing of the distal end of the femur is approxi-
Ž.
mately 150￿ Brinkman,1981.Long axis rotation
of the femur is less prevalent,but has a very
Ž
important role Rewcastle,1977,1980;Brinkman,
.
1981.No equivalent of forearm rotation exists in
Ž.Ž.
the crus Landsmeer,1990 Fig.3.The knee is
essentially a simple hinge joint and is restricted to
Ž
flexion-extension movements Rewcastle,1980;
.
Brinkman,1981.Femoral retraction primitively
Ž
occurs in a near-horizontal plane Rewcastle,
.
1983,with the crus moving in a near vertical
plane,resulting in a force with potential posterior
and lateral components,since the knee describes
an arc about the acetabulum in a horizontal plane.
Displacements of the center of mass thus tend to
be horizontal rather than vertical.Also,func-
tional limb length is less than total limb length
Ž.
because of limb flexure at the knee and elbow
Ž.
Rewcastle,1981.Thus,in the sprawling gait the
orientation of the axes of the major limb joints,
relative to the parasagittal plane,alters during
retraction.Such a situation dictates that certain
movements must occur and certain configurations
must be brought about if posterior thrust is to be
generated.This largely occurs in the hindlimb by
Ž.
crus long axis rotation Fig.3,but,unlike in the
forelimb,the tibia and fibula are not free to move
independent of each other and so must move
Ž.
essentially as a unit Landsmeer,1990.
The knee joint of sprawling lizards is markedly
Ž.
asymmetrical Rewcastle,1977,1980 and the
cruropedal articulation is modified to permit
Ž
simultaneous flexion-extension and rotation Fig.
.
3,rather than the dominance of flexion-exten-
sion typically seen in the wrist or at the ankle
Ž.
joint of mammals Barnett,1970.The pes of
sprawling lizards is markedly asymmetrical,due to
the offset position of the fifth digit and the un-
equal lengths of the first four.
In sprawling lizards the femoral long axis is
directed anterolaterally at the beginning of the
Ž.
stance phase Brinkman,1981;Rewcastle,1983,
the crus is vertical and the metatarsus is directed
Ž.
anteriorly Brinkman,1980,1981.As retraction
proceeds,the femur swings back,out and down so
that its long axis comes to lie at right angles to
the body long axis and becomes depressed
between 20 and 40￿ below the horizontal plane
through the acetabulumwhen the femur is roughly
Ž
perpendicular to the body long axis Snyder,1954;
.
Rewcastle,1983.Femoral backswing thus results
in a reorientation of the knee joint axis so that it
Ž
lies parallel to the body long axis Rewcastle,
.
1983.As the knee joint does not allow rotation
of the crus,the crus rotates on the pes to result in
an orientation of the crural long axis perpendicu-
Ž.
lar to the pedal long axis Fig.3.Without the
rotatory movements that occur at the knee and
ankle,the lower limb elements would not be able
to produce caudally directed thrust.Pedal plantar
Ž.
flexion Fig.3 is important as it enables the pes
Ž
to act as an additional limb lever Brinkman,
.
1981.
Net hindlimb movement occurs in a plane in-
clined fromlateroventral to dorsomesial.The body
Ž
does not pass directly over the limb support as it
.
does in ‘typical’ mammals and thus vertical dis-
Ž
placement of the centre of mass is small Rewcas-
.
tle,1983.This largely eliminates a suspensory
phase in locomotion and restricts lizards to sym-
Ž.
metrical gaits Sukhanov,1968.Locomotor adap-
tations in lizards have thus radiated within the
confines of these inherent limitations,just as
mammalian adaptations have radiated in theirs.
Lizards are generally adapted for moving rela-
tively rapidly in terms of body lengths per unit
Ž.
time Liem,1977,and small lizards are able to
develop great speed while running quadrupedally,
Ž
but usually only over short distances Huey and
.
Hertz,1982.The maximum speed recorded for a
quadrupedal lizard is 9.7 m s
￿1
for Callisaurus
Ž.
Sukhanov,1968.A specimen of Cnemidophorus
sexlineatus reportedly ran at 8.04 m s
￿1
for over
Ž.
one minute Hoyt,1941.With increasing speed a
greater proportion of body weight is borne by the
hindlimbs.
These general principles,established on the
basis of the examination of relatively few taxa,
provide the framework for further integration of
morphological characteristics of various taxa and
their potential locomotor specializations.This re-
quires a fuller understanding of kinematics and
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112 95
the development of a research program in which
specific and explicit questions are posed.Kine-
matic studies essentially allow variations in gait to
be quantitatively documented,building upon a
basic knowledge of movement patterns and gait
characteristics of tetrapods.
5.Locomotor kinematics
Movement in terrestrial tetrapedal vertebrates
is brought about by the actions of four,or rarely
two,limbs and a corresponding shift in the center
of gravity.The two main phases of limb activity
Ž.
are propulsion stance,support and recovery
Ž.
swing,transport,and together they constitute a
Ž.
full limb cycle stride.Support time refers to the
duration of contact,and transport time is the
time of recovery phase.The relationship between
Ž.
support and transport times duty factor is very
specific,with respect to the mechanics of each
limb,and provides the rhythm of limb action.The
locomotor cycle encompasses the completion of
Ž.
all four limb cycles Sukhanov,1968.
During terrestrial quadrupedal locomotion in
lizards the limbs work in diagonal pairs or in a
symmetrical diagonal sequence.The characteris-
tic gait of both lizards and urodele amphibians is
a symmetrical trot in which contralateral fore and
Ž
hind limbs alternate in body support Rewcastle,
.
1981.Various classifications of the tetrapedal
locomotor repertoire of lizards have been pro-
Ž.
duced.Croix 1929 identified three forms of loco-
motion in lizards:a slow walk in the lateral se-
quence;the reptilian trot;and the bipedal run.
Ž.
Howell 1944 suggested that the trot was the
basic locomotor pattern for quadrupedal lizards,
Ž.
and Snyder 1952 lent further credence to this.
Ž.
Sukhanov 1968 differentiated three forms of
locomotion in lizards:a quadrupedal walk,where
the diagonal forelimb leaves the ground before
and touches down before the diagonally opposite
hind foot;a quadrupedal fast gait,in which the
diagonally opposite hindfoot lifts off the substrate
after the forefoot but precedes it in touching
down;and the bipedal gait,outlined above.Ur-
Ž.
ban 1965 indicated that in teiids,however,the
hindlimb may lift before the diagonally opposite
forelimb.
Ž.
Urban 1965 investigated quantitative aspects
of lizard locomotion in the Teiidae,a group cho-
sen because of the great size range exhibited and
the array of locomotor repertoires present,from
quadrupedal to bipedal and limbless types.He
Ž.
Urban,1965 found that inclination of the body
with respect to the substratum alters with chang-
ing gaits and with speed,as it does in iguanids
Ž.
and agamids Barbour,1926;Snyder,1952.With
any one gait type,the faster the lizard,the greater
Ž.
the angle.Urban 1965 also reported that the
hind limbs are more fully straightened in bipeds
than in quadrupeds and this was expressed quan-
titatively in terms of the height of the acetabulum
above the substratum as a percentage of snout-
vent length.This relative measure was found to
increase with increasing speed.The angle that the
femur makes with the body long axis was mea-
Ž.
sured Urban,1965 for a variety of teiids and it
was found that in fast-moving forms the femur
moves from a horizontal to a more vertical posi-
tion as speed increases,bringing the long axis of
the femur closer to the midline.These results
Ž.
were also noted by Irschick and Jayne 1999.
This was not found to be the case with relatively
slowly moving teiids,nor was it the case for
Ž.
Sceloporus clarkii Reilly and Delancey,1997a,b
Ž.
see below.
The gaits of teiids were quantified by measur-
Ž
ing certain parameters of footfall patterns Urban,
.
1965.The ratio of the distance between the fore
and hind feet to snout-vent length was used to
obtain the relative values of distances between
ipsilateral feet.The slow walk gives a large dis-
tance,but as the gait becomes faster the distance
becomes smaller and then increases again as the
Ž
feet begin to overlap the process of overstepping,
.
see Padian and Olsen,1984.Negative values
occur when the pes falls behind the manus and
positive values are given when the pes falls in
advance of the manus.
Following these initial studies,Renous and
Ž.
Gasc 1977 outlined a research program for in-
vestigation of lizard locomotion,summarized
below,that has essentially been overlooked.Re-
consideration of this program may be prudent as
the study of saurian locomotor kinematics moves
forward,as it provides a framework for the inte-
gration of morphological and biomechanical data
that will probably prove to be reciprocally illumi-
nating in comparative studies.Atomization of or-
ganisms into functional components or kinematic
data sets must ultimately lead to re-synthesis if
evolution and function at the whole organism
level are to be understood.
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Ž.
Renous and Gasc 1977 studied the teiid,
Tupinambis nigropunctatus and attempted to inte-
grate morphological data with observed locomo-
tor behaviour to produce a holistic picture.They
began with a biometric study and examined the
relationship of the length of the humerus to that
of the femur across a wide variety of lizards.They
then cross-correlated these measurements with
other standard body measurements and examined
the relative length of each limb segment against
these parameters.To this they added general
descriptions of the osteological and myological
components of the locomotor system,concentrat-
ing on Tupinambis.The study was then restricted
to the pectoral girdle and appendage,the muscles
of which were divided into ‘functional’ assem-
blages,the groupings loosely following those of
Ž.
Gasc 1963.
Locomotion in Tupinambis was studied by way
of cinematography and cineradiography.Footfall
patterns were determined,using the terminology
Ž.
of Sukhanov 1968.Kinematic analysis was ac-
complished by superimposing cinematographic
and cineradiographic images.Translation and ro-
tation at joints was considered,and the functional
aspects of muscles were extrapolated from their
morphological form and calculations of their
physiological cross-sectional area.From these
data,force estimations for each muscle were cal-
culated.Geometric representation of form was
constructed for all muscles considered and aver-
ages presented.The musculoskeletal component
of the pectoral locomotor system was thus ren-
dered into an ensemble of mechanical axes,and
centers of movement were related to vector forces
of the muscles.For each phase of movement a
graphical reconstruction was made and the role
of each muscle,in relation to its mechanical
properties,was assessed.Direction,sense and in-
tensity of forces were calculated for all directions
of movement.Retraction and long-axis rotation
of the humerus were documented with respect to
the glenoid,and rotation of the radius about the
long axis of the antebrachium was also demon-
strated.The role of joint structure in guiding
locomotor movements was discussed.The com-
Ž.
plementary study of Landsmeer 1984 unfortu-
nately overlooked the contribution of Renous and
Ž.
Gasc 1977.
Subsequent to these kinematic,and associated
Ž.
electromyographic Jenkins et al.,1983,investi-
gations of the forelimb,attention switched to the
hindlimbs,the perceived generators of the ma-
jority of locomotor thrust.
With the emergence of affordable and ap-
propriate technological applications,such as
high-speed videography and computer software
programs able to integrate timing,angular and
linear displacement data,study of the locomotor
kinematics of lizards has accelerated in recent
years.Although only a relatively few studies em-
ploying quantitative approaches to limb and axial
kinematics of lizards have so far been published
Ž
Reilly,1995,1998;Reilly and Delancey,1997a,b;
.
Fieler and Jayne,1998;Irschick and Jayne,1999,
the variance in kinematic details between species,
and between speeds within species has already
indicated that the simple description of planti-
grade foot posture and sprawling limbs is not
sufficient to encapsulate the versatility of the
Ž.
sprawling gait Fieler and Jayne,1998.It is be-
coming increasingly evident that the functional
and anatomical diversity of lizard locomotion is
much broader than has heretofore been recog-
Ž.
nized Reilly,1998,and a renewed examination
of the relationship between locomotor perfor-
mance measures and morphological variability is
now in order.
To date,the majority of quantitative kinematic
studies have been devoted to lizards that display a
relatively ‘normal’ pattern of limb morphology
Ž
robust,moderately elongate hind limbs bearing
.
relatively long feet and long digits and relatively
high upper limits to the absolute speed of loco-
motion.Examples are:the studies of the locomo-
Ž
tor kinematics of Sceloporus clarkii Reilly and
.
Delancey,1997a,b;Reilly,1998,a taxon advo-
cated to exemplify the essence of sprawling loco-
Ž.
motion Reilly and Delancey,1997a;Reilly,1998;
Ž.
Dipsosaurus dorsalis Fieler and Jayne,1998,
again taken to be a rather generalized lizard for
the purposes of locomotor studies;and a cluster
of relatively rapidly-moving taxa running at close
to their maximal sprinting speeds ￿ Dipsosaurus
dorsalis,Callisaurus draconoides,Uma scoparia,
Ž
and Cnemidophorus tigris Irschick and Jayne,
.
1999.Such studies have investigated the effect of
Ž
speed Reilly and Delancey,1997b;Irschick and
.Ž.
Jayne,1999 and incline Jayne and Irschick,1999
on kinematic variables.A major sub-theme of
these studies has been the changes that occur in
kinematic variables as speed is increased from a
Ž
slow to a fast walking trot Reilly and Delancey,
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112 97
Fig.4.Changes in angular kinematic variables of a trot with increase in speed in Sceloporus clarkii.The dotted line represents a speed
of 0.27 m s
￿1
,the dashed line a velocity of 0.476 m s
￿1
,and the solid line a speed of 0.833 m s
￿1
.The x-axis is identical for all four
Ž.Ž.
panels and indicates the percentage of stride duration from right pes down 0% to the next placement of the same pes 100%.The
vertical lines on all four panels indicate the time of foot up for each velocity,fast medium and slow,from right to left.The curves have
been smoothed and,for the ankle angle,have been averaged for the time period in which the limb in swung towards the camera during
Ž.Ž.
the swing phase arrowheads.Modified from Reilly and Delancey,1997b:Fig.2.See that paper for more details.
.Ž.
1997b Fig.4,and from a slow walking trot to a
Ž
run including bipedalism if this is attainable by
the species in question ￿ Irschick and Jayne,
.Ž.
1999 Fig.5.This partial emphasis on rapid
locomotion has been justified in the context that
these rapid speeds are ecologically relevant to the
species concerned and capitalizes upon the con-
siderable effort that has been expended over the
last two decades in documenting maximal sprint
Ž
speeds in a wide array of lizard species e.g.Van
Berklumet al.,1986;Bauwens et al.,1995;Irschick
.
and Losos,1998;Bonine and Garland,1999.
Complementing such studies has been the work
Ž.
of Farley and Ko 1997 dealing with the energet-
ics of lateral undulation during the locomotion of
lizards.This study revealed that at low speeds
lizards use their limbs as inverted pendulums,
while at high speeds a bouncing gait is adopted
and the limbs behave in a spring-like fashion,
Ž.
confirming the predictions of Cavagna et al.1997
Ž.Ž.
Fig.5.Changes in angular kinematic variables against time for a quadrupedal left and bipedal right stride of Dipsosaurus dorsalis.
Ž.
Angular displacement,in degrees is indicated on the y-axis and percentage of stride cycle on the x-axis from foot down 0 to 100%.
Ž.
The vertical dashed line indicates the end of the stance phase.Modified after Irschick and Jayne,1999:Fig.6c,d.
( )
A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿11298
Ž.
and Taylor 1978.Energy conservation is a key
factor in the way in which the limbs operate at
different speeds and shifting the center of mass
during lateral undulation accounted for relatively
Ž
little of the total cost of locomotion Farley and
.
Ko,1997.
Lateral body undulation plays an important
part in saurian locomotion and is integrated with
limb movement.Travelling wave patterns,where
points of maximal bending pass down opposite
sides of the body alternately from anterior to
posterior,are most clearly developed in limbless
Ž
terrestrial forms Daan and Belterman,1968;
.
Dobrolyubov,1986.Standing wave patterns,
Ž.
where points of no lateral bending nodes alter-
Ž.
nate with areas of maximal bending internodes
Ž.
Edwards,1977,are clearly developed in forms
Ž
with stoutly developed limbs Daan and Belter-
.
man,1968;Reilly and Delancey,1997a.Standing
wave form varies with the speed of progression
and contributes to increase in stride length
Ž.
Snyder,1962;Daan and Belterman,1968.
In arboreal forms,such as Anolis and Cha-
maeleo,lateral undulatory movements are re-
duced,and in the latter the orientation of the
pectoral girdle on the sternum is vertical rather
Ž.Ž
than horizontal Fig.6.In both Anolis Peterson,
.Ž.
1973 and Chamaeleo Peterson,1984 displace-
ment of the scapulocoracoid on the sternum con-
tributes significantly to stride length in place of
lateral undulation and replaces the whole body
movements of terrestrial forms in enhancing stride
length.
One unusual case of the suppression of lateral
undulatory bending in normal-limbed terrestrial
lizards was reported for juveniles of the lacertid
Ž.
Eremias lugubris Huey and Pianka,1977.These
juveniles mimic noxious beetles and walk stiffly
and jerkily while actively foraging,with strongly
arched backs.The adults are larger than the
beetles that the juveniles mimic,and have a nor-
mal undulatory component in their locomotion.
The juvenile ‘arch walk’ may have evolved from
the facing-off posture sometimes employed by
adult E.lugubris in aggressive encounters.The
kinematic profile of this unusual juvenile gait
would be instructive in understanding the poten-
tial for decoupling axial and appendicular me-
chanics in the context of the sprawling posture.
From the studies outlined above a generalized
but variable picture of the kinematics of lizard
locomotion is emerging.Over a three-fold change
Ž
￿1
.
in speed 0.270￿0.833 m s the majority of
timing variables for Sceloporus clarkii decreased
Ž.Ž.
Fig.6.Diagrammatic representations of the relationships between the glenohumeral articulatory plane ghp in a sprawling lizard a
Ž.Ž.
and a chamaeleon b in relation to the plane of the coracosternal articulation csp.These patterns are associated with different
Ž.
methods of support of the body by the pectoral girdle c,d,with the coracosternal articulation being loaded in compression in the
Ž.Ž.Ž.
sprawler c and in tension in the configuration displaying more erect limbs d.In the latter the clavicles clav are absent and are
replaced functionally by a tensile ligament system.Arrows indicate directions of loading.Other abbreviations:c,coracoid;csa,
coracosternal articulation;hum,humerus;icl,interclavicle;ribc,rib cage;s,scapula;ss,suprascapula;st,sternum;and vc,vertebral
column.
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112 99
Ž
with speed in real time Reilly and Delancey,
.
1997a,b,but the extent and ranges of angular
movements did not change.Increase in speed was
attributed largely to relatively faster femoral re-
traction and knee flexion during the stance phase.
Such a pattern was reported previously for the
Ž
salamander Dicamptodon Ashley-Ross,1994a,b,
.
1995.
The question of how kinematics change with
speed over a seven-fold range of speed changes
Ž
￿1

0.50￿3.50 m s in Dipsosaurus dorsalis Fieler
.
and Jayne,1998 revealed that 27 of 46 kinematic
variables exhibited significant changes.At higher
speeds the femur became markedly adducted dur-
ing the stance phase,raising hip height and,
together with postural changes in the lower limb
segments,increasing effective limb length,thus
enhancing celerity.In contrast,Reilly and De-
Ž.
lancey 1997b found no change in femoral ad-
duction across the range of speeds that they ex-
amined.
These observations generally accord with the
hypothesis that lizards are capable of utilizing two
different forms of limb configuration for different
Ž.
types of progression Rewcastle,1981.In slow
Ž.
locomotion,climbing see below and in locomo-
tion on shifting substrates the hind limb extends
in a near horizontal plane and the body is held
Ž.
close to the substrate Rewcastle,1981.In fast
locomotion on a level substrate,however,the
femur is markedly adducted during retraction and
the body is held clear of the substrate.The mor-
phology of the hip joint permits this transition
Ž.
Vialleton,1924;Rewcastle,1981.
The proximal femoral condyle has a convex
surface and a compressed oval outline.With the
femur held horizontally,perpendicular to the
sagittal body axis,the oval axis is inclined from
anterodorsal to posteroventral.An axis perpen-
dicular to this determines the principal axis of the
Ž
hip joint the axis about which femoral retraction
.
proceeds.The principal motion of the femoral
condyle in the acetabulum is a slide,resulting in
Ž.
femoral swing retraction.The femoral condyle,
however,can also spin within the acetabulum,
resulting in conjoint axial rotation of the femur.
Both types of motion influence the orientation of
Ž.
the knee joint axis Fig.3.Two types of femoral
motion can occur.In the first,femoral retraction
proceeds in a horizontal plane and results in slow
or scansorial type locomotion.In the second,fe-
moral motion is in a non-horizontal,non-parasa-
gittal plane,and is characteristic of fast locomo-
Ž.
tion Snyder,1949,1952;Urban,1965.
Such studies have revealed that as speed in-
Ž.
creases,duty factor decreases Fig.7.The swing
phase decreases at a slower rate and ultimately
stabilizes in terms of timing,while the stance
phase continues to diminish.In fast locomotion
the duty factor may be reduced to only 25% of
Ž
stride duration Honnegger and Heusser,1969;
Reilly and Delancey,1997b;Reilly,1998;Fieler
.
and Jayne,1998.
Ž.
Irschick and Jayne 1999 further documented
change in kinematic variables with speed by in-
vestigating four species of iguanoid lizard and one
species of teiid moving at a variety of velocities,
including close to their maximum sprint speeds
Ž
such that those taxa capable of bipedal locomo-
.
tion adopted this posture.They found that at
high speed the angular variables most important
for separating species were knee angle at the end
of the stance,toe orientation at footfall,mini-
mum and maximum femoral retraction,minimum
Ž.
Fig.7.Relationship of duty factor as a percentage of stride y-axis to velocity for the gekkonid Eublepharis macularius using a slow
walking trot.
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112100
Ž.
femoral depression adduction and minimum fe-
moral rotation.Increasing femoral depression oc-
Ž
curs in Sphenodon with increasing speed Robb,
.
1977,so it is probable that this shift is a primitive
feature of lizards in general.Whereas the kine-
matics of walking and running form a continuum
within species,there is considerable variation in
the details of kinematics from species to species.
Furthermore,different suites of kinematics distin-
guish bipedal from quadrupedal strides in those
species exhibiting bipedalism,and bipedalism rep-
resents a kinematically distinct mode of progres-
Ž.
sion Irschick and Jayne,1999.
In such investigations footfall patterns have
been noted to change with increasing speed.In
Sceloporus clarkii the pes reportedly struck the
substratum either heel-first or in a plantigrade
Ž.
fashion Reilly,1995;Reilly and Delancey,1997a,
while in Dipsosaurus dorsalis running at higher
Ž
speeds,footfall was often digitigrade Fieler and
.
Jayne,1998,in association with a more adducted
femur.Digitigrady was also noted in the fast-run-
ning species examined by Irschick and Jayne
Ž.
1999 at higher velocities,and by Daan and Bel-
.
terman,1968 for Lacerta.Thus,digitigrady may
be associated with other aspects of limb design
Ž
such as relative limb length and especially rela-

tive length of the metatarsus see Garland and
.
Losos,1994;Miles,1994 and may be directly,
although facultatively,associated with high speed
running.
Differences in footfall pattern were also noted
with respect to the orientation of the digits.At
low and moderate speeds in Sceloporus clarkii the
fourth digit was oriented laterally at foot down,
with the first three digits facing more anteriorly
Ž.
Reilly and Delancey,1997b.This orientation did
not change across the moderate range of speeds
examined.The direction of movement was ap-
Ž
proximately aligned with the third digit Reilly,
.
1995;Reilly and Delancey,1997a.At faster
speeds orientation of the long axis of the pes
changed by almost 50￿,pointing almost directly
anteriorly at 2.50 m s
￿1
in Dipsosaurus dorsalis
and reducing the amount of laterally directed
Ž.
thrust Fieler and Jayne,1998.In Uma scoparia,
however,the pes at near maximal sprinting speed
did not achieve this orientation but instead re-
mained directed laterally approximately 20￿ from
Ž
the mean direction of travel Irschick and Jayne,
.
1999.The ability of the pes to display different
angles of placement relative to the mean direc-
tion of travel must again involve adjustments at
Ž.
the mesotarsal joint Fig.3,which is constructed
so that flexion and extension bring about conjoint
Ž.
rotation Rewcastle,1983.The kinematics and
morphology of the ankle require further investi-
gation if variance in pedal angle is to be ex-
plained in species to species comparisons.
Ankle mechanics are also involved in pedal
plantar flexion.At slow to moderate speeds,Reilly
Ž.
and Delancey 1997b reported that pedal plantar
flexion did not contribute significantly to increas-
ing speed in Sceloporus clarkii and that there was
no transition to more erect posture.The last third
of stance is dominated by pedal plantar flexion in
Ž.
Sceloporus clarkii Reilly and Delancey,1997a,
during which time it plays a major role in thrust
Ž.
production.The model by Rewcastle 1983 of the
pes in plantar flexion rolling towards its mesial
border and resulting in essentially posteriorly-
directed thrust along the metatarsophalangeal line
has been questioned by Reilly and Delancey
Ž.
1997a,and a significant amount of lateral thrust
has been proposed as a result of the orientation
of the pes.In this regard,pedal geometry and
force production needs further investigation,and
needs to be integrated with patterns of foot place-
ment and the configuration of pedal skeletal ana-
tomy.
The final thrust of the hind limb takes place
through the claws of those digits remaining in
contact with the substratum ￿ digits one to three
Ž
in Sceloporus clarkii Reilly,1995;Reilly and De-
.
lancey,1997a,and digits two to four in lacertids
Ž.
Arnold,1998.At the end of the stance phase,
Ž
the hind limb may be fully extended lacertids,

see Arnold,1998,or not Sceloporus clarkii,see
.
Reilly and Delancey,1997a.
Axial bending exhibited no change across a
￿1
Ž
range of speeds from 0.27 to 0.833 m s except
.
for snout displacement in Sceloporus clarkii.The
form of axial bending is that of rough standing
Ž
waves,with nodes at the girdles Reilly and De-
.
lancey,1997a.Axial bending contributes to fe-
moral protraction on one side and,simultane-
ously,retraction on the other,and may contribute
up to 20￿ of the femoral protraction￿retraction
arc on each side.
The understanding of kinematics of the lizard
hind limb has been extended to movement on
inclines and in climbing.Data on these types of
locomotion are currently quite sparse,however,
especially for quantitative kinematics.Jayne and
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112 101
Ž.
Irschick 1999 examined the kinematics of hind
limb movements on uphill and downhill inclines
of 30￿ and compared these to locomotion on level
terrain.They noted that the amount of femoral
retraction was similar on all inclines,but that the
degree of femoral rotation varies,indicating that
retraction and rotation can be decoupled.
Hip height was kept at a lower level while
moving on inclines in Dipsosaurus dorsalis,and
this resulted in a lowering of the center of mass
Ž.
Jayne and Irschick,1999.This was accomplished
by reducing the effective limb length by placing
the ankle more lateral to the hip and lessening
the degree of femoral adduction and knee exten-
Ž.
sion Jayne and Irschick,1999.Uphill strides on
a 30￿ incline were shorter and more rapid than
those for equivalent velocities on a level surface
Ž.
in Dipsosaurus dorsalis Jayne and Irschick,1999.
The kinematics of locomotion on all three sur-
Ž.
faces 30￿ uphill,level and 30￿ downhill were
distinct and sprawling limb posture has been ad-
vocated to enhance the ability to move on inclines
Ž.
Rewcastle,1981;Jayne and Irschick,1999.
Ž.
Arnold 1998 also noted that in climbing lacer-
tids the femur does not pass dorsal to the crus.
Ž
Incline and speed have interactive effects Jayne
.
and Irschick,1999.
For climbing-proper,the only kinematic con-
siderations available to date are those of Arnold
Ž.
1998,who made comparative qualitative obser-
vations on lacertid lizards specialized for terres-
trial and climbing locomotion.In climbing,with
Ž.
the aid of claws,on vertical surfaces Arnold 1998
noted that the forelimbs take on a greater impor-
tance as their grip,in head-up situations,is neces-
sary to prevent the lizard from falling outward,
away from its support.Species that habitually
climb display a greater equality of fore and hind
Ž.
limb length Arnold,1998 and the forelimbs con-
tribute much more to total thrust production.A
qualitative account of limb movement in the
gekkonid Tarentola annularis,involving running
on a horizontal trackway,was furnished by
Ž.
Mohammed 1992 ￿ only preliminary kinematic
data are yet available for climbing in gekkonids
Ž.
Zaaf et al.,2001.
Ž.
In terms of limb kinematics,Arnold 1998
noted that the swing phase of climbing lacertids is
very brief,being only one-quarter to one-eighth
as long as the stance phase.The former fraction
was recorded for fast climbing,and although it
represents a relative reduction of the swing phase,
it is still exceeded by the stance phase by a wide
margin,quite unlike the situation seen in terres-
trial locomotion at moderate and high speeds
Ž
Reilly and Delancey,1997b;Fieler and Jayne,
.
1998;Irschick and Jayne,1999.
The biomechanics of climbing vs.terrestrial
locomotion were considered in a different way by
Ž.
Zaaf et al.1999,who compared various aspects
of the biomechanics of the locomotor muscles of
two gekkotans,Eublepharis macularius,a terres-
trial form,and Gekko gecko,a climber.They
noted that in the climber the forelimbs become
more important in the production of locomotor
thrust and the maintenance of grip,and docu-
mented more powerful shoulder retractor muscles
in Gekko than in Eublepharis,and higher flexion
moments across the elbow,preventing the animal
from falling backwards when on vertical surfaces.
These observations parallel the qualitative obser-
Ž.Ž.
vations of Arnold 1998.Zaaf et al.1999 noted
that climbers should benefit from relatively
shorter limbs and a more sprawling gait in order
to keep the center of mass close to the substrate.
The consideration of comparative lever arm me-
chanics of muscles of the shoulder and forelimb
Ž.
Zaaf et al.,1999 echos another part of the
comprehensive research program outlined by
Ž.
Renous and Gasc 1977,but was again presented
without reference to the latter.
At slow speeds three or four limbs support the
animal,but as speed increases fewer limbs are
required to support the body simultaneously,and
the support pattern drops to two or even one
limb.How the pattern is generated and altered is
not well understood.For lizards little information
is available concerning differentiation experi-
ments and the role of central locomotor mecha-
Ž.
nisms Grillner,1975.Whether movements are
due to the activity of central elements only,or
whether peripheral reflex loops play a role is
Ž.
largely unknown.Steiner 1886 transected the
spinal cord of lizards at the thoracic level and
found that the hind limbs still exhibited the full
repertoire of locomotor movements.When sti-
muli were applied to the tail,walking movements
were initiated that continued after the stimulus
Ž.
ceased.Kenins 1977 demonstrated that a true
stretch reflex is present in the muscles of the hind
limb of the scincid Tiliqua,the response being
Ž
mediated monosynaptically Kenins et al.,1970;
.
Kenins,1972,1977 and resembling the mam-
Ž.
malian pattern Kenins,1977,and differs signifi-
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A.P.Russell,V.Bels ￿Comparati
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e Biochemistry and Physiology Part A 131 2001 89￿112102
cantly from the weak response of anurans.The
stretch reflex arc in Tiliqua may play a role in the
maintenance of posture and in the servo-control
or servo-assistance in the performance of move-
Ž.
ments Kenins,1977.It thus appears that the
spinal cord houses the central pattern generator,
which controls each limb.The actual phasic activ-
ity in each cycle is coordinated with the other
generators by coordinating interneurons,and the
central generator can also phasically open and
close different reflex pathways.The combination
between each pair of limbs can thus be altered by
regulating them to be in or out of phase with
Ž.
each other Grillner,1975.
The neural control program of limb movement
among tetrapods is quite conservative,with adap-
tive changes in locomotion occurring primarily
through mechanical and physiological modifica-
Ž.
tions of bones and muscles Reilly,1995.The
Ž
spinal quotient the relative cross-sectional size of
.
the spinal cord at the pectoral and pelvic regions
vs.the interlimb region was investigated by Giffin
Ž.
1990,who found a relationship between the type
of locomotion and the neural processing capacity
associated with this.Terrestrial sprawling lizards
were employed as a baseline measure against
which to compare taxa with other locomotor
modes.Basiliscus,a facultative biped,was found
to have a normal pectoral spinal quotient,but an
enlarged pelvic one.The aquatic Amblyrhynchus
had lower pectoral and pelvic quotients than did
terrestrial sprawlers,as did the limb-reduced
Scincus.The arboreal Chamaeleo and the volant
Draco had the highest pectoral and pelvic
Ž.
quotients,which Giffin 1990 associated with ma-
nipulative and postural behaviors,respectively.
Ž.
Focusing on teiids,White and Anderson 1994
examined size-dependent variation of stride
parameters and locomotor patterns across seven
species.Axial measures were found to conform to
geometric similarity,while limb segments exhib-
ited negative allometry.Variations recorded for
the relationships between stride length,stride fre-
quency and duty factor were found to represent
locomotor specializations and were not simply
size-dependent.These data were then used to
estimate the mass-specific energy cost per stride,
with the finding that differences between taxa are
probably due to a combination of ecological cir-
cumstance and body size.The relationships
between locomotor costs,ecological circumstance
and body dimensions are complex,and such con-
founding factors as the potential for elastic en-
ergy storage are essentially unknown for lizards
Ž.
White and Anderson,1994.
For Varanus komodoensis,the largest living
Ž.
lizard,Suzuki and Hamada 1992 found that all
four of the feet were in contact with the sub-
stratum for one-quarter of the time during walk-
ing,and hypothesized that this extensive time of
contact was associated with gigantism and the
support of great weight.They found that in-
creased musculature rather than bone compen-
sates for weight support in this taxon.Among
Ž.
varanids,Christian and Garland 1996 found that
the larger species have longer limbs relative to
snout-vent length,but relatively shorter feet and
thicker limbs.
6.Bipedalism
The phenomenon of bipedal locomotion in
lizards has received considerable attention,begin-
Ž.
ning with the observations of Cope 1875 on
Ž.
Basiliscus
￿
ittatus,and de Vis 1884 and Saville-
Ž.
Kent 1895,1896 on Chlamydosaurus kingi.Sav-
Ž.
ille-Kent 1896 employed photographic tech-
niques before they had been applied to the analy-
Ž.
sis of quadrupedal saurian gaits Marey,1901,
and also Saville-Kent,1896 analyzed trackways
and reported that Chlamydosaurus becomes tri-
Ž.
dactyl digits two,three and four in contact at
high speeds.Subsequent to this Saville-Kent
Ž.
1897 reported bipedalism in Physignathus
leseuerii and Amphibolurus muricatus,and pre-
dicted a widespread parallel distribution of
Ž.
bipedalism in iguanids.He Saville-Kent,1898a,b
then switched his attention to iguanid lizards,and
by 1902 the phenomenon of bipedalismwas known
Ž.
to be widespread Saville-Kent,1902.Annandale
Ž.
1902 described bipedalism in the agamid Calotes
Ž.
￿
ersicolor and Thomas 1902 in Lacerta
￿
iridis.
Since these early reports the phenomenon of
bipedalism has been more thoroughly investi-
Ž.
gated.Sukhanov 1968 indicated that lacertilian
bipedalism is not significantly different from
quadrupedalism and that it should be considered
as a variant of quadrupedal locomotion ￿ a fast
trot with dominance of the hind limbs.Kinemati-
Ž.
cally,however,Irschick and Jayne 1999 have
more recently demonstrated that quadrupedalism
and bipedalism display some fundamental me-
chanical differences.
( )
A.P.Russell,V.Bels ￿Comparati
￿
e Biochemistry and Physiology Part A 131 2001 89￿112 103
Ž.
Snyder 1949 described the bipedal gait of
Basiliscus basiliscus,based upon cinematographic
analysis,noting that in each step cycle the center
of gravity changes and compensatory adjustments
are continuously made.A small amount of com-
pensation occurs via swinging of the forelimbs,
but most occurs by way of pitching motions of the
trunk and the movement and posture of the heavy
tail.The distal end of the femur describes an
ellipse during locomotion,with equal segments
being described anterior and posterior to the
acetabulum.The major portions of the ellipses
described by the distal ends of the crus and pes,
however,lie posterior to a perpendicular drawn
through the acetabulum and in this region most
of the thrust is produced.The thigh,crus and pes
all participate actively in propulsion,but the most
powerful muscles bringing about retraction of the
leg reside in the base of the tail.When parts of
Ž.
the tail were removed Snyder,1949 the effec-
Ž.
tiveness of bipedalism was altered.Snyder 1949
stated that these manipulations illustrated the
importance of the tail as a counterbalance,but
Ž.
Du Brul 1962 felt that such manipulations may
have also disrupted some of the neural feedback
mechanisms responsible for locomotor coordina-
tion.It is likely that a critical mass of the caudife-
moralis muscle mass was removed,thus limiting
Ž.
the effectiveness of femoral retraction Fig.8.
Following his manipulative and observational
Ž.
study,Snyder 1952 undertook a comparison of
quadrupedal and bipedal locomotion in lizards,
using Crotaphytus collaris as his quadrupedal ex-
ample.He concluded that in bipeds the rapid trot
merges into a bipedal gait as speed increases,an
observation more recently corroborated by Chris-
Ž.Ž.
tian et al.1994a,b and Irschick and Jayne 1999.
Not all bipeds are able to move with the same
Ž.
degree of efficiency,and Snyder 1952 indicated
that the agamid Amphibolurus cristatus is able to
attain a much more pendulum-like action of the
hind limb than is possible in Basiliscus.This dif-
ference is brought about by the ability of Amphi-
bolurus to depress the femur further from the
horizontal and results in less body rotation during
running,a smaller degree of lateral deviation of
the pes when the ground is first struck,and a lack
of rotation of the pes on the substrate during the
propulsive stroke.The ellipses described by the
distal ends of the femur,crus and foot also indi-
cate a greater degree of efficiency of gait in
Ž.
Amphibolurus than in iguanids Snyder,1952.All
Ž.
Fig.8.The caudifemoralis musculature cfb,cfl of Iguana
iguana and related musculature of the pelvic and thigh regions
in ventral view.Abbreviations:a,ambiens;af,adductor fe-
moris;cfb,caudifemoralis brevis;cfl,caudifemoralis longus;
cfltc,crural tendon of the cfl;ft,femorotibialis;ftet,tendon of
the flexor tibialis externus;ftg,femorotibial gastrocnemius;
fti2,part 2 of the flexor tibialis internus;hi,hypoischium;if,
Ž
iliofemoralis;pife,puboischiofemoralis externus parts a1,a1,
.
a3 and b;pifi2,3,parts 2 and 3 of the puboischiofemoralis
internus;pil,puboischiadic ligament;pit,puboischiotibialis;
pt,pubotibialis;and ta,tibialis anterior.
of these observations and inferences suggest that
a comparative examination,both qualitative and
quantitative,of the hip structure in a variety of
bipedal lizards would prove to be instructive.
The common elements of habitat associations
with saurian bipedal locomotion were considered
Ž.
by Snyder 1952.Bipeds can be divided into two
general groups ￿ primarily terrestrial species
living in open,sandy or rocky areas and lizards
living in brushy or forested areas that may be
classed as arboreal or semi-arboreal.The quanti-
tative differences in myology and osteology of
quadrupedal and bipedal lizards were considered
Ž.
by Snyder 1954 and a general summary of
Ž.
saurian bipedalism presented Snyder,1962.
For the most part,bipedalism in lizards has
been related to rapid locomotion in the context of
Ž
escaping from predators see references cited
above plus Ruthven,1912;Osborn,1916;Bar-
bour,1926;Burt,1931;Boker,1935;Loveridge,
¨
1945;Svihla and Svihla,1952;Reed,1956;Belkin,
.
1961;Snyder,1967.This escape behaviour at-
tains one of its most extreme manifestations in
Basiliscus,which is able to move bipedally ‘across’
( )
A.P.Russell,V.Bels ￿Comparati
￿
e Biochemistry and Physiology Part A 131 2001 89￿112104
the surface of water in its escape endeavours.
Ž.
Laerm 1973 analyzed this phenomenon with the
aid of high speed cinematography.The aquatic
gait was noted to be similar to the terrestrial
bipedal gait,but with more pronounced vertebral
flexion and pelvic girdle rotation.The differences
Ž.
noted were interpreted Laerm,1973 as being
directly associated with the nature of the sub-
strata,greater ‘slippage’ of the foot being permit-
ted by the lower resistance offered by water when
compared with a solid substratum,resulting in
compensatory movements.On a solid substratum
limb retraction accounts for approximately 65%
of total body displacement and girdle rotation
Ž.
approximately 35% Laerm,1973.In water the
comparable figures are 33 and 67%,indicating
the importance of an increased amplitude of the
lateral undulatory waves and of the resulting gir-
Ž.
dle rotation Laerm,1973.Within the genus
Ž.
Basiliscus Laerm,1974 the functional size of
adaptive features within and between species is
related directly to the way in which they are able
to provide for support and propulsion.Allometric
changes in the functional size of such features
were found to correlate with observed habitat
preferences and the ability for running ‘on’ water.
Hydrodynamic drag,resulting from the form of
the elongate pes,orientation of the digits,pres-
ence of lateral toe fringes and the speed at which
the lizard moves,provide the forces necessary for
support of Basiliscus on water.While toe fringes
were not necessary for locomotion ‘on’ water
Ž.
Laerm,1973,they do enhance the efficiency of
Ž.
this locomotor strategy Laerm,1974.That the
toe fringes are not necessary is also exemplified
by the behaviour of juvenile green iguanas that
have been observed to run bipedally ‘over’ the
Ž
surface of water Laerm,1973;Burghardt et al.,
.
1977.
Analysis of filmed sequences reveal that
Basiliscus does not run ‘over the surface’ of the
water,but rather runs ‘through’ it,maintaining a
considerable proportion of the body above the
Ž.
surface Laerm,1973.The degree to which the
animal is submerged during these locomotor bouts
is the result of the combined interaction of speed
Ž.
and body mass Rand and Marx,1967.The pedes
of Basiliscus slap the surface of the water and
then stroke downward,thus expanding an air
cavity from which the foot is pulled before the
Ž.
cavity collapses Glasheen and McMahon,1996a.
Small individuals generate relatively much larger
Ž
forces than large ones Glasheen and McMahon,
.
1996b and an upper limit of size that can effec-
tively employ this mode of progression may thus
be set by these relationships.It may,in part,
explain why juvenile but not adult green iguanas
Ž
have been observed to display this behavior see
.
above.Bipedal aquatic locomotion has also been
Ž
reported for Uranoscodon Hoogmoed,1973;
.
Howland et al.,1990,Laemanctus and Anolis
Ž.
Barbour and Ramsden,1919.
In varanids bipedalism may also be involved in
Ž.
defensive posturing.Loveridge 1934 illustrated a
tripodal defensive stance in Varanus gouldii,in
which the erect body is balanced on the hind legs
and tail.This was also discussed by Barbour
Ž.Ž.
1943.Allen 1972 reported such posturing in
this species as a component of intraspecific ritual-
Ž.
ized combat.Murphy and Lamoreaux 1978 de-
scribed bipedal defensive posturing in Varanus
mertensi and similar bipedal defensive posturing
Ž
has been reported for Varanus bengalensis De-
.Ž.
raniyagala,1958,V.giganteus Waite,1929 and
Ž.
V.sal
￿
ator Honnegger and Heusser,1969.
7.Other locomotor modes and modifications
Methods of locomotion in lizards vary accord-
ing to the nature of the substrate.As well as
locomotion on relatively solid substrates,utilizing
two or four limbs,many lizards are able to swim
Ž
Cowles,1946;Tercafs,1961;Sukhanov,1968;
.
Dawson et al.,1977.No aquatic adaptations oc-
Ž
cur in the limb structure of living lizards Romer,
.
1956.Generally during swimming the limbs are
held adpressed to the body and lateral undulation
of the body and tail provides the propulsive force
Ž.
Tercafs,1961;Guibe,1970.This mechanism of
´
propulsion has been referred to as sculling
Ž.Ž
Seymour,1982 and axial-subundulatory Braun
.
and Reif,1982.The only taxa recorded to em-
ploy the limbs to effect progression in water are
Ž.
Tarentola mauritanica Gekkonidae,Chamaeleo
Ž.
dilepis Chamaeleonidae,and the scincid Trachy-
Ž.
dosaurus rugosus Tercafs,1961.
Most notable among taxa that swim habitually
is the marine iguana,Amblyrhynchus.No physio-
logical or morphological modifications for aquatic
Ž
locomotion have been reported Dawson et al.,
.
1977,the partially webbed feet and laterally
compressed tail not differing significantly from
those of Iguana iguana.The tail of Hydrosaurus is
( )
A.P.Russell,V.Bels ￿Comparati
￿
e Biochemistry and Physiology Part A 131 2001 89￿112 105
Ž
extremely modified to this end,however Seymour,
.
1982.In terms of swimming efficiency in Amb-
Ž.
lyrhynchus,Vleck et al.1981 found some onto-
genetic differences,the cost of transport for
swimming marine iguanas decreasing as body mass
increases.At similar speeds the cost of swimming
is approximately 25% of the cost of walking in
Ž.
Amblyrhynchus Gleeson,1979,indicating an en-
ergetic advantage to be gained from swimming
Ž.
Seymour,1982.Hatchling Amblyrhynchus have
variable terrestrial escape velocities,with those
achieving the highest speeds having relatively
Ž
longer tibiae and shorter pedes Miles et al.,
.
1995.This result is discordant with that for most
lizards,where a relatively longer metatarsus is
associated with the highest sprint speeds,but may
be connected with the unusual habitat occupancy
of this taxon.
Sphenomorphus quoyii employs swimming and
diving as predator escape responses,and uses the
tail as the propulsive device during swimming
Ž.
Daniels,1985.If the tail is automized,swimming
Ž
and diving efficiency are greatly reduced Daniels,
.
1985.
Many lizards excavate burrows by way of a
variety of modifications.The great length of the
forelimbs of the iguanid Chalarodon is a modifi-
Ž.
cation for burrowing Blanc,1965.The gekkonid
Ptenopus garrulus digs burrows in loose sand with
the aid of lateral fringes of elongate scales
Ž.
bordering the digits Brain,1962.Sand is loosen-
ed with the forefoot on one side then kicked back
Ž
with the hind foot of the same side Haacke,
.
1975.
Ž.
Luke 1986 reviewed the functional mor-
phology and evolution of lizard toe fringes.Al-
though they are often cited as an adaptation to
locomotion on shifting sand,they may have a
variety of functions,even within the same individ-
Ž.
ual Luke,1986.In a broadly comparative study,
Ž.
Luke 1986 divided fringes into four types,ac-
cording to the form of their constituent scales
Ž.
Luke,1986;Figs.1￿4.In some species more
than one fringe type is found on a single toe,
particularly when medial and lateral aspects of
the digits are compared.She concluded that
fringes have evolved independently at least 26
times,in seven families of lizards.Variation in
fringe morphology shows a strong correlation with
Ž.
substrate type.Carothers 1986 demonstrated ex-
perimentally that the toe fringes of the iguanid
lizard Uma scoparia enhance locomotor perfor-
mance on loose sand.Both acceleration and ve-
locity are significantly adversely affected by their
removal.
Palmatogecko digs with webbed feet rather than
fringes.Sand is loosened and scooped backwards
first by the manus,and then the pes of the same
side reaches forward and pushes the sand further
Ž.
back Haacke,1976;Russell and Bauer,1990.
The closely related Kaokogecko lives in gravel
plain areas and excavates with webbed feet in a
Ž.
similar fashion Steyn and Haacke,1966,but
debris may be clasped with the pes and deposited
further back,rather than being moved just by
Ž.
pushing Haacke,1976.No kinematic profiles of
limb-based burrowing in lizards are available.
Sandswimming also occurs in a variety of lizards,
with body movements very similar to those seen
Ž
in swimming in water Cowles,1941;Sukhanov,
.
1968.Sand burial techniques in 23 species of the
Ž.
iguanid Liolaemus Halloy et al.,1998 revealed
three distinct modes of burial ￿ sandswimming,
vertical burial,and head-first burial.These modes
differ primarily in the movements of the head and
tail,with limb use across taxa remaining relatively
constant.
A return to undulatory movement is seen in
Ž
many forms showing limb loss or reduction Es-
.
sex,1927;Stokely,1947;Gasc,1968;Lande,1978.
Many lizards are able to climb well by means of
Ž.
claws Russell,1976;Arnold,1998;Zani,2000,
Ž
grasping feet Camp,1923;Boker,1935;Gasc,
¨
.
1963;Peterson,1973 or subdigital adhesive pads
Ž
Dellit,1934;Mahendra,1941;Maderson,1970;
.
Russell,1975.Climbing is normally carried out
using normal alternating limb movements
Ž.
Sukhanov,1968;Russell,1975.
The semi-erect posture,found in chameleons
Ž.
Peterson,1973,1984 and rapidly moving cro-
Ž.
codilians Zug,1974;Webb and Gans,1982 is
associated with a greater amount of humeral de-
pression during the propulsive stroke than is found
Ž.
in sprawlers Bakker,1971.In the semi-erect
stance the humerus makes an angle of up to 65￿
with the horizontal,the important difference be-
ing associated with the structure of the glenoid
cavity.Here the long axis of the glenoid slants up
and back and the overhanging scapular lip can
brace the upward thrust of a more vertically ori-
ented humerus as the latter undergoes backswing
Ž
in a more vertical orientation Bakker,1971;Pe-
.
terson,1973,1984.Coupled with this,the more
vertical the humeral backswing,the less effective
( )
A.P.Russell,V.Bels ￿Comparati
￿
e Biochemistry and Physiology Part A 131 2001 89￿112106
humeral long axis rotation becomes in increasing
stride length and a correlate of this is a reduction
Ž.
in humeral torsion Lecuru,1969.Movement at
´
the elbow is more restricted to simple flexion-ex-
Ž.
tension Peterson,1973,1984,and a similar situ-
ation is seen in the femur of semi-erect forms
Ž.
Bakker,1971.
The semi-erect humerus requires less muscular
bracing,but the forearm more than in the sprawl-
ing gait because the slope is more ventromedial
Ž.Ž.
Gray,1944 and less vertical Bakker,1971.In
chamaeleons the shift from a sprawling to a
semi-erect stance is associated with a narrowing
of the trackway,in connection with movement
along branches of narrow diameter.This is fur-
ther associated with the grasping modifications of
Ž.
the manus and pes Gasc,1963.Modifications in
the antebrachium of chamaeleons permit manual
contact to be maintained while the humerus
Ž
moves through its semi-erect arc Peterson,1973,
.
1984.
Ž.
Jumping between branches Sukhanov,1968
Ž.
and as a means of predator escape Russell,1977,
Ž
occurs,even in limbless forms Cliburn,1957;
.
Bauer,1986.The kinematics of jumping in Anolis
Ž
carolinensis Bels and Theys,1989;Bels et al.,
.
1992 reveal that hindlimb posturing prior to
take-off and the take-off itself are highly stereo-
typed,but the landing is highly variable.Both
Ž.
parachuting Russell,1979;Russell et al.,2001
Ž
and true gliding Colbert,1967;Russell and Dijk-
.
stra,2001 are also employed in association with
jumping behavior.
8.Prospectus
Sufficient information is now available on both
the anatomical specializations associated with the
sprawling gait of lizards and the kinematics of
movement to begin to unite these avenues of
study into a more holistic comparative program.
Sufficient data exist to indicate that considerable
variation in kinematic patterns exists within
species as velocity changes and between species
to suggest that locomotor morphology may be a
major determinant of kinematic patterns.Com-
parative studies combining morphological and
kinematic investigations may help to unravel the
subtleties of locomotor ecomorphology as ex-
pressed within and between lizard clades.
Ž.
As Renous and Gasc 1977 endeavoured to
stimulate,there should now be the commence-
ment of an overarching research program with
specific and explicit questions.While there will
continue to be contributions about individual
species,chosen out of expediency rather than
because they help elucidate a particular problem,
greater focus on questions that can be viewed in a
phylogenetic context will ultimately prove to be
more informative.Initial progress in this regard
Ž.
has been made by Irschick and Jayne 1999,with
Ž.
a major focus on kinematics and by Arnold 1998,
with a major focus on morphology and niche
occupancy.The next phase should be to combine
these complementary approaches so that morpho-
logical and kinematic variables and variability can
be better understood.
Much recent work has focussed on hindlimb
kinematics and it might well be timely to augment
this approach with a renewed focus on the fore-
Ž.
limb.Landsmeer’s 1980,1983,1984 contribu-
tions provide a firm morphological foundation for
such considerations,especially when placed in the
context of scapulocoracoid-sternal mechanics and
the variety of morphologies that they display
Ž.
Peterson,1973;Jenkins et al.,1983.The
shoulder region is mechanically quite distinct from
the hip and an integration of the morphology and
kinematics of these regions within and between
species will prove profitable.Recently extensive
use has been made of skeletal variation in the
shoulder region of lizards as a source of syste-
Ž
matic characters,e.g.Lang,1989;Frost,1992;
.
Reeder and Wiens,1996;Holingsworth,1998,
but little is known of the functional significance
of these various anatomical arrangements.Such
features may relate to aspects such as humeral
posture and gait characteristics.Tantalizing
Ž
glimpses have been given in this regard Werner
.
and Broza,1969;Gasc,1963;Peterson,1973,but
little in the way of mechanics or kinematics is
understood.Comparative aspects of glenoid
Ž.
structure and humeral depression Bakker,1971,
Ž.
and humeral morphology Lecuru,1969 have
´
been outlined,but have yet to be placed into a
robust phylogenetic and functional context.
Morphology and kinematics could be more ex-
tensively combined in investigations of the hind
limb as well.An initial outline of the comparative
limb mechanics and their structural correlates
Ž.
was provided by Snyder 1952.Such approaches
could now be amplified and integrated with inves-
Ž
tigations of acetabular morphology as begun by
( )
A.P.Russell,V.Bels ￿Comparati
￿
e Biochemistry and Physiology Part A 131 2001 89￿112 107
.
Vialleton,1924 and its relationship to femoral
depression.There is preliminary evidence of dif-
ferences in these aspects between major clades of
Ž.
lizards Snyder,1952 that can now be addressed
in a more rigorous phylogenetic context and com-
pared kinematically via quantitative analyses.Such
approaches,as well as complementary ones on
quadrupedal locomotion,could also be combined
with force-plate applications in order to investi-
gate the magnitude and direction of thrust pro-
duction from the highly asymmetrical lacertilian
pes.Controversy exists here,for example,in the
predictions from morphology made by Rewcastle
Ž.
1983 and the implications gleaned from tread-
mill-based running resulting from the work of
Ž.
Reilly and Delancey 1997a.
Kinematic profiles of lizards moving at a variety
of speeds,including slow,steady locomotion,could
be more extensively employed to investigate ve-
locity-based changes within and between taxa,
and these could be combined to investigate as-
Ž.
pects of energy conservation Farley and Ko,1997
and the potential for elastic energy storage and
Ž.
return White and Anderson,1994.For the most
part,investigation of the latter is precluded for
many lizards because of their overall small size
and the small ligaments that they possess.One
candidate for investigation might be,however,the
long tendon of the caudifemoralis longus muscle
that runs to the crus and crosses the knee joint
Ž.
Fig.8.General attention to arthrology would
also be informative.
The interactive effects of incline and speed on
locomotor kinematics have begun to be investi-
Ž.
gated Arnold 1998;Jayne and Irschick,1999,
but have not yet been fully explored in the con-
text of climbing and scansorial locomotion.Pre-
liminary hints of what such foci of investigation
may have to offer are provided by Zaaf et al.
Ž.
2001,but it will be important to ask questions of
lizards allowed to move in circumstances,and
upon surfaces,compatible with their normal loco-
motor repertoire and capabilities.Such ap-
proaches,combining kinematics,morphology and
electromyography,will be able to determine
whether,for example,axial and appendicular con-
Ž.
tributions to locomotion Huey and Pianka,1977,
and femoral retraction and long axis rotation
Ž.
Jayne and Irschick,1999 can be decoupled in
different locomotor circumstances,and if so,how.
Ž.
The saurian ankle is complex Russell,1993
and its operation relative to foot orientation and
thrust production have not been clearly expli-
cated.Pedal placement upon footfall may or may
Ž
not vary with velocity Reilly,1995;Reilly and
.
Delancey,1997a;Irschick and Jayne,1999.Vari-
ance observed so far may be due to differences in
experimental set up or may be reflective of dif-
ferences in mesotarsal joint structure and ankle
mechanics between lineages.This is another area
in which morphology and kinematics need to be
examined in tandem and in a phylogenetic con-
text.
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Ž.
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