AM. ZOOLOGIST, 2:191-203(1962).
ADAPTATIONS FOR BIPEDAL LOCOMOTION OF LIZARDS
RICHARD C. SNYDER
Department of Zoology, University of Washington
In the course of vertebrate history, four
rather distinct types of bipedalism have
evolved: (1) the reptilian method (thecodonts, dinosaurs, lizards) in which the body
is balanced more or less horizontally over
the legs and the tail acts as a cantilever; (2)
the avian method in which, with obvious
exceptions, the body is balanced horizontally over the legs and the center of gravity is
directly over the hindlimbs; (3) the primate-human method in which the body is
balanced semi-vertically or vertically over
the limbs; and (4) the ricochetal method
of saltatorial mammals in which the body
is also balanced semi-vertically and the
highly modified hindlegs are used simultaneously in repetitive jumping. Bipedal
locomotion has thus evolved independently
at least six times in vertebrate phylogeny;
twice in reptiles (thecodont-dinosaur group,
lizards), once in birds, and three times in
mammals (marsupial ricochet, placental
ricochet, primate alternating gait). It is of
course recognized that several other kinds
of mammals can attain a degree of bipedalism for short periods, but in none of them
is the position maintained, nor the gait
habitually used.
of the selective factors leading to bipedalism in vertebrates as well as certain features of the adaptations of muscle and bone
involved. The archosaurian ancestors of
birds were already bipedal.
The functional mechanics of human locomotion have been analyzed in several
publications (cf Steindler, 1935; Morton,
1952; Elftman, 1954); that of the chimpanzee by Elftman (1944). Differences in the
musculature related to the mode of progression of quadrupedal mammals and man
have been discussed by Haxton (1947). The
locomotion of ricochetal mammals has been
the subject of papers by Elftman (1929),
Howell (1923), Hatt (1932), Bartholomew
and Caswell (1951) and others. Slijper
(1946) has studied vertebral adaptations of
bipedal mammals, both walking and saltatorial. Fisher (1955) has summarized the
major papers concerned with adaptations
of the avian hindlimb for various types of
locomotion; a useful general account is
found in Young (1950). Skeletal and muscular adaptations for bipedal locomotion in
dinosaurs have been discussed by Osborn
(1917), Romer (1923, 1956) and many
others, while bipedalism in living lizards
With the exception of several species of has been studied chiefly by Magne de la
lizards (Snyder, 1952), most birds, and man, Croix (1929, 1935) and Snyder (1949, 1952,
no other living vertebrate regularly pro- 1954).
The reptilian type of bipedalism, as exgresses at the bipedal two-time gait. As
emplified
by modern lizards, is the most
Howell (1944) has pointed out, the bipedal
and,
in terms of economy of acprimitive
walk and run has, except for birds, develtion,
the
most
inefficient
method. The type
oped from quadrupedal methods of locoby
a
standing or movof
posture
assumed
motion and he has briefly discussed some
ing lizard necessitates strong musculature
I am indebted to Thomas H. Frazzetta for helpful
for the maintainance of pose alone when
discussion of the manuscript and for preparing all
the body is off the ground, and lizards genbut one of the illustrations; also to Dr. B. Schaeffer
erally
have large limb bones and limb
of the American Museum of Natural History who
loaned the film of alligator locomotion from which
muscles. In large dinosaurs, this pose was
Fig. 2 B was prepared. This study was supported
probably impossible, particularly if the
in part by a grant from Initiative 171 of the State
gait
was bipedal; the hindlimb has been
of Washington and by Grant RC 8405, P.H.S.
(191)
192
RICHARD C. SNYDER
moved as close to the body as possible for
direct weight-bearing (graviportal). Romer
(1956) has pointed out that in archosaurs
the hindlimb has rotated forward to a position close to the body and has tended to assume a vertical posture. In both saurischian
and ornithischian bipedal dinosaurs the
articular head of the femur is turned sharply inward from the line of the shaft and
there is some development of a femoral
neck; comparable adaptations are found in
birds and man, but not in lizards. The legs
of lizards describe wide ellipsoidal arcs
throughout the locomotor cycle and operate primarily in the horizontal plane. Hindlimb action in lizards is basically the same
in both bipedal and quadrupedal progression (Snyder, 1949, 1952). In mammals,
birds and, probably, bipedal archosaurs,
limb action is in the sagittal plane with
relatively little tendency toward movement
in lateral or medial directions. The basic
differences between lacertilian and mammalian locomotor patterns are based chiefly
on differences in limb posture, the presence
of a large, heavy tail in lizards, and differences in bone and muscle structure of the
pelvis and hindlimb.
The distinct tendency toward bipedalism
in many species of lizards is of particular
interest in that no marked structural
changes between quadrupeds and bipeds
exist. Descriptive, analytic and comparative
studies of the skeletal and muscular structures associated with the bipedal habits of
lizards has formed a basis on which to interpret adaptive divergence from "typical"
lacertilian morphology and has clearly
shown that bipedalism has been achieved
with relatively slight modifications of pelvic or appendicular structure (Snyder,
1954), a situation in contrast to that found
in comparisons between quadrupedal reptiles and bipedal dinosaurs or between
quadrupedal mammals and man. Definite
modifications occur in the girdle and limb
structure of archosaurs which are indicative of bipedal trends (Romer, 1956) and
the differences between girdle and limb
morphology of quadrupedal mammals and
the higher primates are widely known. The
attainment of bipedalism by running lizards involves skeletal and muscular adaptations which, although distinct and definite
in trend, differ only slightly and are more
readily followed than the larger differences
between distantly related species. It is the
purpose of this paper to summarize and
discuss these adaptations.
GAITS AND LOCOMOTOR CYCLE
Four gaits are utilized by lizards; the
walk, running walk, trot and bipedal run,
all symmetrical forms of locomotion. The
basic pattern of limb action in quadrupedally running lizards is the trot, in which
body support is maintained by diagonally
opposite limbs. Since the hindlimbs are
much longer than the forelimbs, the latter
are unable to match them stride for stride,
particularly when speed increases and the
hindlimb stride is lengthened. Two additional factors limit increase in forelimb
stride length. Unlike cursorial mammals
(Hildebrand, 1959) there is no vertical flexion of the spine and the pectoral girdle is
relatively immobile. In the running iguanids (Basiliscus basiliscus, Crolaphytus collaris, C. wizlizeni, Sceloporus undulatus)
and agamid (Amphibolurus cristatus) studied with high-speed cinematography (Snyder, 1949, 1952) the hind foot makes contact with the ground well in advance of the
forefoot except in Sceloporus which is not
bipedal. The hindlimbs are swung around
(lateral to) the forelimbs throughout the locomotor cycle (Fig. 1) and, at speeds above
that of a walk, the front legs never contact
the ground simultaneously as they do in
certain asymmetrical mammalian gaits such
as the gallop and canter. As speed increases,
hindlimb stride is lengthened and the time
intervals of body support on the hindlimb
increases as a smooth transition from quadrupedal to bipedal progression is made.
During rapid quadrupedal running, the
length of hindlimb and forelimb stride is
almost exactly equal to body length (snout-
BIPEDAL LOCOMOTION OF LIZARDS
FIG. 1. Crotaphytus collaris running quadrupedally. Vertebral column strongly flexed in the direction o£ the advanced hindlimb.
vent); but in bipedal running,'-the hindlimb can accomplish a stride three times as
long. The reasons for this are based upon
length of the limb, the distance through
which it is moved, and the distance through
which the acetabulum moves during the
time that the feet are not in contact with
the ground. The rate of stride may increase
slightly or not at all; the maximum observed increase in rate was 10%. Hildebrand (1961) has noted that as the cheetah
accelerates, the stride length is nearly doubled while the stride rate increases but
slightly.
In addition to the factors mentioned
above, length of stride is also a function of
193
the angle of limb swing (the degree to
which it approaches the vertical or horizontal) and the amount of horizontal flexion
of the vertebral column (Fig. 1). In regard
to vertebral flexion, the situation is analogous to the vertical flexion of running
mammals (Hildebrand, 1959). The distance
covered during the suspension phase of the
stride is increased and the duration of the
support phase is augmented; in addition,
the flexible vertebral column provides another joint in the locomotor mechanism.
Since different muscles simultaneously
move different joints in the same direction,
the total movement produced is greater
than that of one joint working alone; independent velocities of each segment combine
additively to produce a higher velocity.
The degree of vertebral flexion increases
with speed, and I suspect that the slight increase in rate of stride during bipedalism
may be attributable to the action of the
vertebral column. The vertebrae contribute to locomotor performance in still another way. Bipedal running is characterized by rotation of the body axis (up to
five degrees from vertical), which tends to
bring the hindfeet toward the mid-ventral
line, a cursorial advantage. It is at present
impossible to judge the effect, if any, of
vertebral rotation on stride length.
It is certain that speed increases with bipedalism. Many authors have indicated
that lizards do not use the bipedal gait unless they are already running at full quadrupedal speed and this may be true under
natural conditions, although Basiliscus,
Amphibolurus and Crotaphytus can assume
the bipedal gait directly from a resting
position or from slow or rapid quadrupedal progression (Snyder, 1952). Information
gathered from the film strips, where film
speed and the distance traveled by the animal are known, indicate the following
speeds converted to miles-per-hour (it is
not possible to say whether the animals
were performing maximally under laboratory conditions):
194
RICHARD C. SNYDER
A
)
y
s
FIG. 2. Locomotor arcs of the distal ends of right
hihdlimb segments of A, Crotaphylus collaris running bipedally; B, Alligator in rapid quadrupedal
walk. Location of acetabulum at intersection of
perpendicular lines. Solid line, femur; dotted line,
shank; broken line, metatarsals (foot). Direction of
progression from left to right. Made from motion
picture by projection.
Species
Basiliscus (young)
Basiliscus (adult)
Crotaphytus
Amphibolurus
Sceloporus
Quadrupedal Bipedal
11
5
5'
5.6
6.8
16.0
12.0
Analysis of the locomotor cycles of Basi-
liscus, Crotaphytus and Amphibolurus, species of comparable running efficiency, show
that mechanisms for bipedalism differ in
interesting ways. In the iguanid genera,
the distal end of the femur describes an ellipse (Fig. 2, A) that is almost equidistant
craniad and caudad of a perpendicular
drawn through the hip joint. The major
portion of the ellipse formed by Amphibolurus is well forward of the hip joint. When
the posterior portions of the ellipses formed
by the distal ends of the shank and foot are
compared, it is evident that in Amphibolurus there is considerably less dorsal and
lateral swinging of the leg segments during
recovery of the limb for the next stride.
The explanation for this difference lies in
the ability of Amphibolurus to maintain
the limbs in a relatively more extended position throughout its locomotor cycle, resulting in placement of the feet closer to
the midline and a more pendulum-like
movement of the leg than in bipedal iguanids. Both adaptations are of advantage to
a cursorial animal in that propulsive leverage is improved and the energy required for
recovery is reduced. Comparison of the locomotor cycle of Alligator with that of lizards
(Tig. 2, B) reveals that limb action in the
former is much more pendulum-like and
that the major phase of the propulsive
thrust takes place posterior to the hip
joint—features to be, expected in an archosaur and certainly a more efficient procedure than that of any lizard studied. The
large size of the lacertilian internal trochanter effectively limits the degree to which the
femur can act in a vertical plane; the trochanteric head is adjacent to and directly
below the head of the femur. In Alligator
the trochanter is small and more clistally
placed; adduction of the thigh does not
force the protruberance against the ischium
as it does in lizards.
FUNCTION OF THE TAIL
Reptilian bipedalism would probably be
impossible without a long, relatively heavy
tail to act as a counterpoise for head and
trunk weight and as a compensating mechanism for shifts in the center of gravity. Each
step of a bipedal vertebrate changes the
center of gravity; in man, compensation for
subsequent loss of balance takes place by
swinging of the forelimbs, and in birds by
back and forth movements of the head and
neck (Howell, 1944). In lizards, adjust-
BIPEDAL LOCOMOTION OF LIZARDS
195
SKELETAL PROPORTIONS
ments are made by a small amount of forelimb swinging and, to a much greater exThe skeletal proportions and modificatent, by movements of the tail. Measure- tions of bipedal lizards have been presented
ments of Basiliscus, Crotaphytus, Amphibo- in detail elsewhere (Snyder, 1954) and will
lurus, Sceloporus and Alligator reveal that be summarized here. The axial skeleton of
the centers of gravity are located in the bipeds is characterized by a decrease in
middle of the trunk (halfway between in- length of the presacral region (head-trunk
guinal and axillary regions). Vertical in- length) and an increase in tail length. Headclination of the body moves the center of trunk length is 23 to 33% of total body
gravity more nearly over the pelvis, and length, while tail length is 65 to 76% in biboth length and weight of the tail are of pedal species; comparable measurements in
importance in enabling the lizard to attain quadrupeds are 30 to 46% and 53 to 68%
and maintain the semi-erect posture. When respectively. Bipedal species are further
the light, terminal segments (between %. characterized by a slightly narrower pelvis
and Yi of the total length) are removed, bi- (interacetabular width), a longer ilium with
pedal lizards are able to elevate the trunk, a better developed preacetabular process
but equilibrium, during running is disturbed and heavier, more solidly fused transverse
to the point where only three to five strides processes of the sacral vertebrae. All bipedseem possible before the animal loses its al species show considerable reduction in
balance and falls (Snyder, 1949, and un- length of the forelimb, and the degree of
published observations). If the posterior reduction is greatest in the manus (Fig. 3);
y2 to y3 of the tail is removed, the lizards slight reductions may occur in the brachium
cannot maintain the bipedal posture for and antebrachium. Modifications of the
more than one step.
hindlimb differ in iguanids and agamids.
The largest and most powerful femoral In the former, there is lengthening of the
retractors, the caudofemoralis muscles, lie hindlimb which involves each limb segment
in the base of the tail. They take origin and the increase is most marked in the
variously from the anterior ten or more proximal segments. The hindlimbs of bicaudal vertebrae, and insert into the tro- pedal agamids show either no elongation
chanteric fossa and crest of the femur. Dur- or, if lengthening occurs, the increase is
ing locomotion, the tail base moves from mostly a function of the pes (Fig. 3).
side to side as alternate femora are retracted; when the thigh is extended and retraction is beginning, the tail base is always toward that side where the most powerful muscle contraction is taking place
(Fig. 1). The remainder of the tail follows
this basal movement in much the same way
that the terminal portions of a whip would
follow movement of the base, but the analogy is not exact since terminal tail motion
can be controlled by the lizard. It is frequently raised or lowered while the animal
is moving and the lateral swinging can be FIG. 3. Diagrams of limb proportions of represenreduced. It has not been possible to make tative bipedal and quadrupedal lizards. Femora
drawn to same size; cms, pes and forelimb segments
exact observations or deductions on the pre- drawn to scale to show relative lengths of appencise role of the tail in the control of bal- dicular segments, f, femur; c, crus; p, pes; h, huance, although it definitely performs this merus; ab, antebrachium; m, manus; Bas, Basiliscus; Crot, Crotaphytus; Ig, Iguana; Seel, Scelopofunction.
rus; Amphi, Amphibolurus.
196
RICHARD C. SNYDER
It has become axiomatic that cursorial
specialization involves an increase in metapodial length and a decrease in the relative
length of the propodial limb segments. In
lacertilians the femur is always longer than
the crus, and it is of interest to note that
the relatively slight increases in limb length
of cursorial iguanids do not change this relationship. The pes is the longest limb segment of all; its increase in bipedal agamids
may or may not be of cursorial significance.
The mass of the distal part of the limb is
an important factor in locomotor performance, for a heavier foot means a greater
force necessary for recovery during a stride,
and this is particularly true for a plantigrade animal whose limbs do not operate
as pendulums. Unless the animal becomes
digitigrade, there would seem to be little
advantage in increasing pes length. In addition, there is considerable evidence that
most cursorial iguanids and agamids are
preadapted for bipedalism; the limbs seem
long enough, forelimb support is reduced
during rapid locomotion and there is reason to suspect that some increase in hindlimb length coupled with a heavier tail in
species such as Uma, Holbrookia, Sceloporus, Uta and Cnemidophorus could result in the adoption of a bipedal gait (Howell, 1944; Snyder, 1952, 1954). The situation
in regard to limb proportions of archosaurs
is, however, reminiscent of conditions
found in mammals. In both bipedal saurischians and ornithischians there is a
strong tendency toward lengthening of the
tibia and an increase in metatarsal length
to form an additional limb joint; the trend
toward metatarsal elongation and the development of a bird-like foot is an archosaurian characteristic not found in other
reptiles (Romer, 1946).
HINDLIMB MUSCULATURE
Investigations on the myology of quadrupedal and bipedal lizards have revealed
that there are no fundamental morphological differences. Angles of attachment,
length of moment arms, and the degree to
which corresponding muscles are composed
of parallel or pennate fibers are quite uniform. The most pronounced modifications
of the hindlimb muscles of bipeds are a
marked increase in the development of crural extensor and plantar flexor musculature
and a reduction in size of the femoral extensor and adductor groups. No significant
differences in development of femoral flexors or pedal dorsiflexors were found. The
crural flexors show a variability difficult to
correlate with what is known about locomotor behavior of lizards, except that in bipeds they are smaller than the extensors—
the reverse of the situation found in quadrupeds. There is some tendency in bipedal
species toward a more proximal grouping
of muscles, although it does not approach
the degree of similar adaptation characteristic of cursorial or saltatorial mammals.
Comparison of lacertilian and mammalian
hindlimb muscles reveal striking differences in the development of the protractor
and retractor groups, particularly the latter. The reptilian caudofemoralis muscles
are unique in providing both power and
speed in femoral retraction; no comparable
mechanical arrangement is found in mammals.
A detailed description of lacertilian hindlimb muscles, comparisons of their relative
development in different specks, and discussions of muscle functions has appeared
in an earlier paper (Snyder, 1954); consequenty, only a brief summary will appear
here. Some instructive comparisons have
been made with the muscles of Alligator
and with certain mammals; in addition, the
caudofemoralis complex has been restudied. A diagram of the muscles of the lizard
hindlimb is presented in Fig. 4.
The femoral flexor (protractor) muscle
(puboischiofemoralis in tern us) shows a variability iri development which, from the
viewpoint of locomotor mechanics, appears
to have little significance. Recovery of the
limb is similar in both quadrupedal and bipedal progression, and the bulk of this
muscle varies from 5 to 9% of the total
BIPEDAL LOCOMOTION OF LIZARDS
197
thigh increases in inverse proportion to the
speed of locomotion. Quadrupedal species
do not attain the speed of bipeds, and it
is significant that their coxofemoral repifi
tractors are larger. It is also significant
that this musculature forms nearly 42%
of
the alligator limb muscles. It may
amb + / '
femtib iff
be noted from examination of the locomotor cycle (Fig. 2) that femoral retraction not only pulls the body forward,
but also raises it; furthermore, rapid locomotion in the alligator is not in the same
class with that of lizards. Although the arrangement of the hip muscles in crocodilians is different from that of lacertilians,
the caudofemoralis muscle is similarly
placed and is the most powerful retractor
of the thigh.
Examination of this musculature in agamids reveals that in Amphibolurus, the femoral retractors are astonishingly large
(36%; 32% for caudofemoralis alone), and
in Agama the femoral extensors comprise
28% of the hindlimb musculature. The biFIG. 4. Diagram of lizard hindlimb muscles. Arpedal locomotor cycle of Amphibolurus inrows indicate direction of muscle pull, amb, amvolves
operation of the thigh mostly antebiens; cfb, caudofemoralis brevis; cfl, caudofemoralis longus; edb, extensor digitorum brevis; edl, rior to the hip joint (Snyder, 1952), and reextensor digitorum longus; fdb, flexor digitorum
traction is less pronounced in scope; the imbrevis; fdl, flexor digitorum longus; femtib, femoroplication
may be that femoral retraction is
tibialis; fte, flexor tibialis externus; fti, flexor tibialis internus; gast. gastrocnemius; ictr, ischiotromore powerful and contributes to propulchantericus; ilf, iliofemoralis; ilfib, iliofibularis;
sion to a greater degree than in other liziltib, iliotibialis; per, peroneus; pife, puboischioards.
femoralis externus; pifi, puboischiofemoralis internus; ta, tibialis anterior; VA, vertebral axis.
The adductor musculature (adductor femoris, puboischiotibialis) is reduced in biweight of the hindlimb muscles. The alli- peds (6.6 to 8.0%); that of quadrupedal lizgator flexor falls within this range (8%). ards varies from 8.3 to 10.5%. Reduced imThe femoral extensor (retractor) muscula- portance of adductors is also characteristic
ture (puboischiofemoralis externus, iliofe- of mammals and of the alligator (4.9%),
moralis and caudofemoralis longus and whose limbs tend to operate in the sagittal
brevis) bulks largest in quadrupedal igua- plane. Placement of the feet toward the
nids. This functional group comprises 23% midline in lizards is almost entirely a funcof the total musculature of Crotaphytus, tion of body rotation during locomotion.
27% for Basiliscus and about 30% for IguaThe crural flexor muscles (flexor tibialis
na and Sceloporus (Fig. 5). Since femoral internus and externus, iliofibularis and
retraction involves not only the action of pubotibialis) comprise between 13.3 and
these muscles, but also the forward momen- 19% of the limb musculature (Fig. 5), and
tum of the body when the lizard is run- are important in the quadrupedal locomoning, it appears that the muscular force tion of all species. They are smaller in the
necessary to bring about retraction of the alligator (12%) than in any lizard. The
198
RICHARD C. SNYDER
25
50
45
2 0 —,
40
35
I 5
30
25
I 0
20
I5
I0
5
5
B
C
Am A g
I
FEMORAL EXTENSORS
E)
All
c
A 1
Anr Ag
CRURAL EXTENSORS D
CRURAL FLEXORS EH
25
25
20
20
I 5
I5
I0
C
I 0
—
GAST.
8
C
1
S
PLANTAR
Am Ag
All
FLEXORS
B
Am Ag
All
ADDUCTORS
FIG. 5. Comparative proportions (ratios of dry weights) of appendicular muscle groups to the
total weight of the hindlimb muscles. B, Basiliscus; C, Crotaphytus; I, Iguana; S, Sceloporus;
Am, Amphibolurus; Ag, Agama; All, Alligator; gast, gastrocnemius muscle alone.
crural extensors (ambiens, iliotibialis and
femorotibialis), however, particularly the
femorotibialis, are conspicuously larger in
bipedal iguanids (femorotibialis size for
Basiliscus and Crotaphytus is 12.8 and
11.5% respectively; 6.1 and 5.6 for Iguana
and Sceloporus and 5.4% for Alligator).
The crural extensors provide a large part
of the force that propels the body forward
and upward, and also function to check
and control forward momentum. Measurements of these muscles in seven bipedal and
four quadrupedal iguanids indicate that
the degree of development is correlated
with body weight (Snyder, 1954), but there
is another significant factor operating in
the use and development of the crural musculature that should not be overlooked.
The lizard hindlimb operates as both a propulsive lever and (when the limb is retracted) as a propulsive strut. In the former action, power is exerted at right angles
to the long axis of the limb; when the femur is retracted, the limb is subjected to a
bending strain. Consequently, in addition
to strong hip extensors there must be strong
BIPEDAL LOCOMOTION OF LIZARDS
199
tive pattern involves elongation of each
hindlimb segment and increased development of the plantar flexors. Hindlimb
lengthening in agamids, when present, occurs primarily in the pes and is associated
with hypertrophy of the caudofemoralis
muscles. These differences are reflected to
some degree in the locomotor arcs of the
appendicular segments.
There is a slight tendency toward a more
proximal grouping of limb musculature
and a corresponding increase in tendon
length in bipedal lizards (Fig. 6). The functional effect of this arrangement is that the
distal portions of the limb segments are
lightened and can be moved through the
locomotor arc with relatively less expenditure of energy, but this feature may well be
cancelled by the greater leg length of most
bipeds. Bipedal species utilize quadruped
methods of locomotion most of the time,
and while it seems certain that proximal
muscle grouping is a cursorial adaptation,
I hesitate to term it a bipedal one.
As indicated, the most powerful femoral
No significant differences in the pedal retractors, the caudofemoralis longus
dorsi flexor musculature (tibialis anterior, muscles, take origin from the base of the
peroneus brevis, extensor digitorum com- proximal caudal vertebrae and insert into
plex) were found. Of the pedal plantar flex- the trochanteric fossa and crest of the feors (gastrocnemius, peroneus longus, flexor mur. These muscles extend between tail
digitorum complex), the gastrocnemius is base and femur in a way that gives them
slightly larger in bipedal lizards (bipedal great power; Howell (1944) has stated that
iguanids, 9.6 to 12.3%; quadrupedal igua- both reptiles and birds can retract the thigh
nids, 8.5 to 9.9%; bipedal agamids, 7.6%; with greater force than is probably possible
quadrupedal agamids 6.1%). In Crotaphy- in mammals with comparable proportions.
tus, the muscle is conspicuously large In all lacertilians studied, the main tendon
of insertion passes ventral to the femur, and
(12.3%); in Alligator it is small (6.4%).
It is important to emphasize that muscle an additional long tendon extends the
modifications which are important in a length of the thigh and attaches to the capgiven type of adaptation are not equally sule of the knee joint (Fig. 7). This tendon
manifested in all species that display a com- is also present in crocodilians and in Spheparable degree of that adaptation. The cau- nodon. Careful dissections, manipulations
dofemoralis complex is very large in Am- and tetanization of this muscle were perphibolurus, very small in Crotaphytus, and formed on Sceloporus, Crotaphytus and Alintermediate in other bipeds; a trend to- ligator in an attempt to determine the funcward a reversal of this tendency is charac- tion of the long tendon and the precise acteristic of the gastrocnemius. Yet all biped- tion of the muscle. The hindlimb of freshly
al species are capable of comparable effi- anesthetized animals was skinned, the cruciency in bipedalism. The iguanid adap- ral flexors removed, and the sciatic nerve
muscles to prevent passive extension of the
knee and ankle, a condition met by powerful two-joint muscles, the crural flexors and
plantar flexors. In bipedal locomotion the
limb is used as a propulsive lever, a propulsive strut, and as a control to the forward and downward momentum of the
body; the latter two actions are performed
by the caudofemoralis longus, femorotibialis, and gastrocnemius. It is therefore significant that the crural flexors are less powerful than the extensors in all bipedal species studied, and that the reverse is true of
quadrupeds except for Agama (Fig. 5).
Reed (1956) reported one instance of temporary bipedal progression in Agama caucasica and it is possible that A. stellio may
use it occasionally. Haxton(1947) discussed
the similar arrangement of the limb
muscles of man, and pointed out that the
act of checking forward momentum is more
important than the use of the limb as a propulsive lever; the hamstring muscles are
relatively less powerful than in quadrupedal mammals.
200
RICHARD C. SNYDER
nip.
FIG. 6. Superficial ventral musculature of the left hindlimb of 1, Basiliscus; 2, Crotaphytus and
3, Sceloporus to show tendency toward proximal muscle grouping in bipedal species, at, adductor
libialis; pit, puboischiotibialis; pi. apo, plantar aponeurosis. Other abbreviations as in Fig. 4.
severed; in some cases the crural extensors
were also severed. The caudofemoralis
muscle was exposed from origin to femoral
and popliteal insertions and tetanized with
a standard battery inductorium at submaximal levels of stimulation. Results, on both
lizards and the alligator were as follows:
1 When the thigh was protracted and
held immobile in the normal position assumed at the beginning of the propulsive
stride, stimulation caused a slight crural
flexion and both shank and foot were
drawn toward the midline. There was a
definite and strong pull on both tendons.
When the thigh was freed, shank flexion
plus powerful retraction of the thigh retulted and the foot was pulled toward the
body during the motion.
2. When the thigh was directed laterally
and the crus partially extended, contraction of the muscle exerted tension through
both tendons and the long tendon was
pulled outward and away from the femur.
Crural flexion was not as pronounced as be-
FIG. 7. Lateroventral view of the vertebral column, pelvis and hindlimb of Crotaphytus to
show the caudofemoralis longus muscle (cfl) and its insertions.
BIPEDAL LOCOMOTION OF LIZARDS
201
FIG. 8. Semidiagrammatic ventral view of the pelvis and proximal left hindlimb of Crotaphytus
to show attachments and probable actions of the caudofemoralis longus muscle. Tendons, solid
black; AB, direction of muscle pull; CD, length of moment arm. Left, limb protracted; middle,
limb protracted and long tendon cut; right, limb partly retracted. See text for explanation.
fore, but there was a strong femoral rotation (the bone rotated about its axis in a
forward direction, thus drawing the crus
and foot posterior).
3. When the thigh was placed in the
fully retracted position with crus extended
or flexed, muscle contraction had no effect
on the long tendon which remained flaccid;
all the force of contraction was exerted on
the femoral head which was now fully rotated. No shank flexion occurred.
4. When the long tendon was cut, muscle
stimulation caused femoral retraction and
rotation as before, but there was of course
no action on the crus.
The force exerted on the long tendon of
the caudofemoralis longus causes the tendon to bow outwards when the thigh is in
the forward or lateral position during locomotion. The effect is to increase the length
of the moment arm and cause a more powerful onset of retraction than would other-
wise result if the tendon were not present
(see Fig. 8). As the thigh moves laterally
and caudally, tension on this tendon becomes progressively less, but progressively
greater on the femoral tendon. The caudofemoralis muscles thus operate to overcome
initial inertia and to provide most of the
force for limb retraction. If the long tendon were not present, the onset of retraction would be mechanically less efficient;
most of the effort would be delivered when
the length of the moment arm was at its
maximum (when the pull on the femur is
at an angle of 90°). In this connection, considerations of the relative effectiveness of
the long tendon at different limb positions
refer directly to the moment arm, and only
indirectly to the force of limb movement,
since the latter depends not only on the
moment arm but also on the amount of tension in the muscle which probably varies
with limb position. Nevertheless, it appears
202
RICHARD C. SNYDER
certain that the function of the caudofemoralis is rapid and powerful femoral retraction, rotation of the thigh, and fixation
of the cms.
It appears certain that femoral retraction
and crural extension contribute most of
the propulsive power in lizard locomotion.
The foot is not constructed in a way to permit efficient plantar flexion, nor is the position it is forced to assume through the locomotor cycle conducive to application of
maximum leverage; while it may be applied to the ground in a nearly straight
(cranio-caudal) line at the onset of propulsion, it tends to rotate laterally as the limb
moves through the propulsive phase of the
stride. Nevertheless, plantar flexion does
occur to some degree, and it appears significant that bipedal species show a slight
modification which increases the angle of
application of the gastrocnemius. The hamate process of the fifth metatarsal is hypertrophied in all bipeds, and is considered
to be a functional analogue of the mamalian calcaneum (Schaeffer, 1941; Snyder,
1954).
In a running biped, the work done in
raising the center of gravity and in accelerating the legs can be minimized if the effect
of the moment of inertia around the acetabulum can be reduced. Smith (1956) has
shown (hat the moment of inertia of the
limb skeleton about the acetabulum can be
reduced without changing the total limb
length if the relative lengths of the distal
segments are increased (thus implying relative reduction of the proximal segments),
or if the distal segments are lightened; both
tendencies are characteristic of cursorial
mammals. Some lightening of the distal
segments is apparent in both bipedal iguanids and agamids, but lengthening of the
limb is marked only in iguanids and takes
place proximally. The effect of the moment of inertia can also be reduced by flexing the limb, which all lizards do, or it can
be overcome by an increase in the muscle
power to move the limb. The increase in
caudofemoralis size of Amphibolu-us night
be interpreted as such an adaptation, but
no comparable tendency exists in any iguanid biped studied. It is probable that the
muscle is already strong enough to meet bipedal needs, and it is certain that it has a
more favorable position for action than any
mammalian femoral retractor.
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