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Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 69:355-375 (1986)
Architectural and Histochemical Diversity Within the Quadriceps
Femoris of the Brown Lemur (Lemur fulvus)
FREDc. ANAPOL AND WILLIAM L. JUNGERS
Departments of Oral Anatomy and Orthodontics, College ofDentistry,
University of Illinois at Chicago, Chicago, Illinois 60612 (I? C.A.);
Department of Anatomical Sciences, School of Medicine, State University of
New York at Stony Brook, Long Island, New York 11794 WL.J.)
KEY WORDS Fiber architecture, Muscle histochemistry, Lemur
fuluus, Quadriceps femoris
ABSTRACT
Physiologically related features of muscle morphology are considered with regard to functional adaptation for locomotor and postural behavior in the brown lemur (Lemur fuluus). Reduced physiological cross-sectional
area, estimated maximum excursion of the tendon of insertion, length of
tendon per muscle fasciculus, and areal fiber type composition were examined
in the quadriceps femoris in order to assess the extent of a “division of labor”
among four apparent synergists.
Each of these four muscles in this prosimian primate displays a distinguishing constellation of morphological features that implies functional specialization during posture and normal locomotion (walWrun, galloping, leaping).
Vastus medialis is best suited for rapid whole muscle recruitment and may be
reserved for relatively vigorous activities such as galloping and leaping (e.g.,
small cross-sectional area per mass, long excursion, predominance of fast-low
oxidative fibers, relatively little tendon per fasciculus). In theory, rectus femoris could be employed isometrically in order to store elastic strain energy
during all phasic activities (e.g., large cross-sectional area per mass, short
excursion, predominance of fast-high oxidative fibers, large amount of tendon
per fasciculus). Vastus intermedius exhibits an overall morphology indicative
of a typical postural muscle (e.g., substantial cross-sectional area, short excursion, predominance of slow-high oxidative fibers, large amount of tendon per
fasciculus). The construction of vastus lateralis reflects an adaptation for high
force, relatively high velocity, and resistance to fatigue (e.g., large crosssectional area, long excursion, most heterogeneous distribution of fiber types,
large amount of tendon per fasciculus); this muscle is probably the primary
contributor to a wide range of locomotor behaviors in lemurs.
Marked dramatic architectural disparity among the four bellies, coupled
with relative overall fiber type heterogeneity, suggests the potential for exceptional flexibility in muscle recruitment within this mass. One interpretation
of this relatively complex neuromuscular organization in the brown lemur is
that it represents an adaptation for the exploitation of a three-dimensional
arboreal environment by rapid quadrupedalism and leaping among irregular
and spatially disordered substrates.
The analysis of muscle function in primate
locomotion is complicated by the vast architectural and histochemical variability that is
found among and within whole muscles. Differences in gross architectural Configuration
0 1986 ALAN R. LISS, INC.
can affect contractile properties of muscles
such as tetanic tension and maximum velocity (Gans and Bock, 1965; Gans, 1982).Other
Received April 19,1985; revision accepted September 13,1985.
356
F.C. ANAPOL AND W.L. JUNGERS
properties, such as time-to-peak-tension and
“fatigability,” appear to be the consequence
of cytological or histochemical differences
among muscle cells (Denny-Brown, 1929;
Burke et al., 1971; Burke, 1981).
Much of the prior work on the relationship
between muscle form and function has emphasized specific aspects of muscle morphology and how myological variation is
associated with differences in locomotor behavior observed among closely related taxa.
These studies include, for example, relative
distribution of muscle mass (Ashton and Oxnard, 1963; Stern, 1971; Fleagle, 19771, the
proportion of tendon composing whole muscles (Alexander, 1974; Alexander and Bennet-Clark, 1977; Biewener et al., 19811, and
relative fiber type composition (Sickles and
Pinkstaff, 1981).
Recent in vivo studies further demonstrate
how architectural and histochemical differences among muscles can account for differences in the contractile properties of whole
muscles as well as how intra- and intermuscular recruitment occurs during mammalian
locomotion (e.g., Gillespie et al., 1974; Armstrong et al., 1977; Goslow et al., 1977; Smith
et al., 1977; Sullivan and Armstrong, 1978;
Taylor, 1978; Walmsley et al., 1978; Smith et
al., 1980; Spector et al., 1980; Walmsley and
Proske, 1981; Anapol and Jungers, 1982;
Gardiner et al., 1982; Muhl, 1982).
The manner in which the wide variety of
myological configurations that can be generated by these several variables contributes
to functional specialization among muscles
remains unclear. For any taxon, the allocation of the “labors of locomotion” among
muscles of a synergistic group may reflect
relatively subtle, yet genuinely distinctive,
requirements for positional behavior. Differences between phylogenetically disparate
species that appear to exhibit similar locomotor repertoires are especially critical in
the recognition of less-obvious requisite differences in adaptation to the environmental
substrate.
In this study of quadriceps femoris in Lemur fuluus, we demonstrate that vastus medialis (VM), rectus femoris UXF), vastus
intermedius (VI), and vastus lateralis (VL)
are each characterized by a unique constellation of physiologically related morphological features, implying fuctional specialization
for each muscle of this synergistic group. Architectural disparity among the four muscles, coupled with overall fiber type
heterogeneity, suggests functional versatility for optimal exploitation of a complex arboreal environment via a locomotor
repertoire dominated by rapid quadrupedalism and leaping among substrates of various
sizes and spatial arrangements Petter et al.,
1977; Ward and Sussman, 1979).
MATERIALS AND METHODS
Morphology
Architectural morphology was studied in
five adult brown lemurs (Lemur fuluus). Two
specimens were obtained from the collection
of the Department of Anatomical Sciences,
State University of New York at Stony Brook.
Three additional specimens were available
after the muscles of the right hindlimb were
removed for histochemical analysis of fiber
type distribution (see below). All were thawed
and fixed by submersion ( 7 4 % formaldehyde, 3% phenol) with one hindlimb set in a
typical quadrupedal postural position as estimated from videotapes and personal observation of live animals (Fig. 1). A total of four
VM and RF and five VI and VL were examined. Each muscle was identified, following
Murie and Mivart (1872), Jo&roy (1962),and
Jungers et al. (19801, and dissected free from
its attachments to the bone.
METATARSOTIBIO-TALAR
METATARSAL
Fig. 1. Approximate postural angles of hindlimbjoints
in Lemur fuluus. H, horizontal;arrow points anteriorly.
357
ARCHITECTURE AND HISTOCHEMISTRYIN LEMUR QUADRICEPS FEMORIS
sured between the proximal myotendinous
junction (MTJ)and the distal MTJ; acute angle of pinnation (Q) with respect to the probable line of action of the muscle (see above);
length of tendon extending from the proximal MTJ of the fasciculus to its proximal
attachment to bone ( 1; and length of tendon
extending from the istal MTJ of the same
fasciculus to its distal attachment to the bone
2
(td).
Fasciculus, proximal tendon, and distal
tendon measurements for the parallel-fibered VM were taken along the estimated
line of action and along the medial and lateral margins of the muscle and were averaged to generate a single value. The muscles
were trimmed of free tendon, blotted dry,and
weighed on a Mettler (H54AR) balance scale.
Reduced physiological cross-sectional area
was calculated for RF,VI, and VL by using
the formula (Schumacher, 1961; after Weber,
1851; and adjusted by Haxton, 1944)
Fig. 2. Measurement protocol for pinnate muscles; If,
reduced physiological cross-sectional
area(cm2) = [mass (gm) x cos Q]!
(1)
[If (cm) x specific density]
tp, td, and 8 are explained in Material and Methods; x
and y are normal to lf and represent portions of the true
physiologicalcross-sectionalarea of the whole muscle.
Gross measurements of the maximum
length of the muscle belly and the maximum
breadth of the belly perpendicular to the
length facilitated choice of sampling sites.
For architectural measurements in pinnate
muscles, bellies were sampled at the normal
intersections of longitudinal' and transverse
planes approximately 1 cm apart. Accordingly, the number of sampling points depended upon the length and width of the
muscle belly. The longitudinal planes more
or less bisected the smaller muscles and trisected the larger muscles. The transverse
planes either trisected or quadrisected all
bellies.
At each sample point, six neighboring fasciculi were measured--three proximal and
three distal to the point; for each variable,
the mean of the six was used in subsequent
calculations. The following parameters were
recorded (Fig. 2): length of fasciculus (lf)mea'Longitudinal planes were parallel to the probable line of
action of the whole muscle defined as a straight line passing
between the midpoints of the proximal and distal attachments
(followingStern, 1971).
where the specificdensity of muscle is 1.0564
gm/cm3 (Murphy and Beardsley, 1974). Because the fibers insert into the tendon at an
angle to the direction that the whole muscle
contracts, the "useful vector" is resolved by
including cos Q in the calculation (Haxton,
1944; Gans, 1982). This is ignored in the calculation for parallel-fibered muscles where
COSQ= 1.
Estimated maximum excursion of the tendon of insertion (h) was calculated from lf
and 0 according to the following equation
(adapted from Benninghoff and Rollhauser,
1952)
h
=
If (cos 0 - dcos" 0
+ n'
- 1). (2)
The maximum coefficient of contraction (n)
(where n = the length of a fiber after contractiodthe length of a fiber a t rest) was assumed to be 70%(Gans and Bock, 1965).
For each muscle, the ratio of the mean total
tendon length (tt = tp + td) to the mean of
fasciculus length plus total tendon length
was calculated.
The proportion of mass to predicted effective maximal tetanic tension (Po)was calculated to compare the priority of muscle force
versus muscle velocity for a given mass (fol-
358
F.C. ANAPOL AND W.L. JLJNGERS
lowing Sacks and Roy, 19821, where Po =
reduced physiological cross-sectional area
(cm') x specific tension of muscle [assumed
to be approximately 2.3 kg/cm2 (Spector et
al., 1980)l.
Measurements and calculations for each
muscle were averaged for four (VM, RF) or
five (VI, VL)animals and standard errors of
the means were computed. For each variable,
coefficients of variation adjusted for small
sample size (V") (Sokal and Rohlf, 1981)were
calculated among the means of the four muscles and are expressed k standard error k,*).
Histochemistry
Three adult male brown lemurs (L. fuluus
subspecific hybrids: 7 years12.25 kg, 3 years1
1.9 kg, 3 years12.15 kg) were killed by cardiac
injection of sodium pentobarbital 20 minutes
after sedation by intramuscular injection of
Ketaset. Muscle tissue was removed from the
centermost portion of each belly and
quenched in isopentane (2-methyl-butane)
previously cooled to approximately - 150°C
with liquid nitrogen. After 20-25 seconds,
the tissue was quickly removed to a straight
liquid nitrogen bath. Histochemical treatments were performed concurrently and
closely followed standard protocols for alkaline and acid myosin adenosine triphosphatase (ATPase) (Guth and Samaha, 1970),
nicotinamide adenosine dehydrogenase-tetrazolium reductase (NADH-TR), and succinate dehydrogenase (SDH) (Dubowitz and
Brooke, 1973).
Because the treatment for myosin ATPase
is pH dependent and variation in pH sensitivity is found among species (Brooke and
Kaiser, 1970), optimal preincubation environments were determined for lemur muscle.
Following preincubation a t pH 10.35, three
levels of staining intensity or myosin ATPase
activity were clearly distinguishable: light
(low activity), dark (high activity), and a n
intermediate level that appeared slightly
lighter than the dark-staining fibers. The
low-activity fibers were presumed to be slow
contracting fibers and the high- and intermediate-activity fibers were presumed to be
fast contracting (Guth and Samaha, 1970;
Burke et al., 1971; Peter et al., 1972).Following preincubation at pH 4.35, slow fibers exhibited high activity while the activity of the
fast fibers appeared to be inhibited.
When sections are treated for NADH-TR or
SDH, three levels of staining intensity again
are distinguishable (following Stein and Padykula, 1962; Henneman and Olson, 1965):
light (low concentration of reactive product),
medium, and dark. However, these do not
necessarily correspond to the three cell types
that are present following alkaline myosin
ATPase treatment (Nemeth and Pette, 1981).
For the current study, cells that exhibited
medium and high concentrations of oxidative
enzyme were designated highly oxidative
(0).
The quantification of fiber type composition proceeded in the following manner. Two
consecutive sections (one treated for alkaline-stable myosin ATPase and the other for
NADH-TR)were examined under a light microscope to determine whether corresponding
groups of cells were suitable for analysis.
Sections treated for acid-stable myosin ATPase and SDH could be substituted, if necessary, or used to substantiate identifications.
For each alkaline-preincubated myosin ATPase section, deep, middle, and superficial
regions at varying mediolateral locations
were selected. A field was projected onto a
Sharp Linytron-plus color monitor receiver
(XR-3019)through a Sony Vititron black-andwhite video camera mounted on a Zeiss (West
Germany) Universal microscope that was fitted with a planapo objective. The monitor
was interfaced with a Tektronix (4632) video
hard copy device. A hard copy was made of
the region of choice and the cells were identified (either by observation of the monitor or
through the eyepiece of the microscope) and
marked slow or fast according to the intensity of myosin ATPase activity. The corresponding region on the NADH-TR slide was
located and the same cells were marked 0 if
highly oxidative.
Superimposing these two classificatory systems, three classes of cells were tabulated
slow twitch-high oxidative (S), fast twitchhigh oxidative (FO), and fast twitch-low oxidative (F). Cross-sectional areas were measured for six cells (with intact boundaries)
from each class represented within a field
with a GrafPen sonic digitizer (Scientific Accessories Corporation). In nonoblique sections, areas of cells were measured directly
in square centimeters. In oblique sections,
the smallest diameter of a cell was measured
as a precaution against distortion (Dubowitz
and Brooke, 1973) and converted to area [A
= pi x (d/2?]. Direct and indirect methods
of area determination were never mixed
359
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
within a single field. The mean areal values
for each class were converted to square micrometers, according to scale.
For each field, the number of cells in each
class was multiplied by the average crosssectional area per fiber for that class. These
lcm
products were summed and each product was
divided by the sum of products to yield the
percentage of cross-sectional area for a class.
For each class of fibers, the percentages of
cross-sectional area for all three fields from
each section were averaged. If more than one
sample was taken from a muscle, the samples were averaged. For each class, the three
animals were averaged to determine the
value for a “composite” animal.
For each class, two-factorial analysis of
variance (Sokal and Rohlf, 1981)was applied
to test the overall significance of differences Fig. 4. Rectus femoris (see Fig. 3 legend). Middle:
among animals and among muscles. The coronal plane.
Mann-WhitneyU-test (Sokal and Rohlf, 1981)
tested for significance of differences between
all possible pairs of muscles for each class of
fibers in the composite animal. For each class the belly one-third to one-half of its length
of fibers, V* f sv*was also computed for the distally. The more anterior portion of the
attachment is fleshy. Distally, the belly tafour muscles.
pers slightly and is truncated before continRESULTS
uing as a flat tendon into the true patella.
Gross morphology
Some of the more anterior muscle fibers atVastus medialis (VM)(Fig. 3) arises from a tach directly to the superior patella (Jungers
circumscribed attachment on the anterior as- et al., 1980) although a small percentage of
pect of the femoral shaft, just distal to the the most anterior of these coalesce with the
head. The most posterior portion of this at- major tendon of insertion.
VM is a parallel-fibered muscle but at first
tachment is by tendinous fibers which join
glance it appears to be pinnate due to the
irregular geometry of the belly. The long fasciculi are oriented from posteroproximal to
anterodistal, which presumably corresponds
to the direction of contraction of the whole
muscle. VM most closely resembles the variety of parallel-fibered muscle described in
Figure 2d in Gans (1982, p. 169).
Although the long sides of VM are more or
less parallel, the ends of the belly are not.
This is because the fasciculi are not all of
Ilcm
equal length and serial replacement of muscle fiber by less-bulky tendon gradually reduces the anteroposterior dimension of the
belly at both proximal and distal ends. The
proximal tendon slightly covers the posterior
margin of the proximal four-fifthsof the belly,
and the distal tendon covers the deep surface
of the anterior margin of the distal two-thirds
of the belly (Fig. 3).
Fig. 3. Vastus medialis, left hindlimb (L. fuluus). Top:
Rectus femoris (RF) (Fig. 4) is a long, tasuperficial surface; bottom: deep surface; proximal attachment is to the right.
pered cylindrical muscle incompletely
1
360
F.C. ANAPOL AND W.L. JUNGERS
sheathed with thick tendon around the distal
two-thirds of the belly. Proximally, it arises
as two separate tendinous elements (not pictured) from the anterior inferior iliac spine
and the cranial margin of the acetabulum
(Jouffroy, 1962). These immediately merge
into a single, round tendon which enters the
proximal end of the belly. This proximal tendon becomes a flattened central tendon
throughout most of the length of the muscle
belly.
The fasciculi radiate distally at an angle
from the central tendon and continue into a
tendinous sheath which envelops all but the
most proximal surface of the muscle belly. As
the belly tapers toward its distal termination, the tendinous sheath continues as a
thick, narrow, flat tendon that passes superficial to the superior patella and vastus intermedius to insert into the true patella. In
coronal section (Fig. 4),RF is bipinnate for
most of its length. However, the fibers that
originate from the distal end of the central
tendon continue in more-or-lessthe same axis
(as this tendon) as they proceed toward the
tapered end of the belly and into the enveloping outer tendinous sheath.
The fleshy fibers of vastus intermedius (vI)
(Fig. 5 ) arise directly from the anterior periosteum of the femoral shaft with no intervening tendon. In sagittal section, the
relatively short, unipinnate fasciculi angle
distally from the femur and terminate in a
dense superficial tendon that covers all but
the most proximal end of the belly. The extrinsic portion of this tendon contains both
the superior and true patellae and crosses
the knee joint to attach into the tibia1
tuberosity.
Vastus lateralis (VL) (Fig. 6 ) is a thick, fusiform muscle that arises from the anterior
a
Fig. 6. Vastus lateralis (see Fig. 3 legend). Middle:
sagittal plane.
crest of the greater trochanter. This attachment is composed of both the ends ofthe most
proximal muscle fibers and the end of a thick
superficial tendon that covers three-fourths
of the proximal surface of the belly. In sagittal section, unipinnately arranged fasciculi
arise from the superficial tendon and angle
distally toward a thick deep tendon that underlies all but the most proximal end of the
belly.
TABLE 1. Sample sizes from lemur for architectural
data (fasciculus length, angle ofpinnatwn,
tendon length)'
Specimen
1
2
3
4
5
Total
Fig. 5. Vastus intermedius (see Fig. 3 legend). Bottom: sagittal plane.
VM
3
3
3
3
12
RF
VI
VL
Total
-
36
18
18
18
18
108
54
54
54
54
54
270
90
123
105
105
99
522
48
30
30
24
132
'VM,vastus medialis; RF, rectus femoris; VI, vastus intermedius;
VL, vastus lateralis.
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
361
Distally, the belly ends abruptly as the deep
tendon continues to its attachment into the
true patella in common with the remaining
quadriceps. Some fibers have been observed
to insert into the superior patella (Jungers et
al., 1980).
Muscle architecture
Sample sizes for whole muscles and fasciculi within muscles that were examined are
presented in Table 1.Means (k standard error of the mean) for the raw measurements
and calculations are also presented for each
muscle in Table 2. Mean fasciculus lengths
range from 1.77 cm in RF to 8.29 cm in VM.
The angles of pinnation are similar among
the three pinnate muscles (RF, VI, VL). More
than a fivefold difference in mass separates
the lightest muscle (VI) from the heaviest
(VL). The largest average tendon length per
fasciculus is found in the bipinnate RF while
the smallest is in the parallel-fibered VM.
The reduced physiological cross-sectional
area accruing to each muscle is also expressed as a percentage of the total quadriceps area. VL is clearly the dominant muscle,
contributing 58.4% of the estimated maximum potential force of the quadriceps. VM
contributes the least to potential force, only
5.8%of the total. Despite its low mass, pinnation allows the potential force contribution
of VI to attain 2.5 times that of the parallelfibered VM. The bipinnate muscle (RF) obtains only a one-third-larger value than does
VI. Thus, pinnation does not necessarily increase potential force in all cases.
With regard to the calculation of maximum
excursion, the wide disparity between VM
and the rest of the quadriceps suggests its
relative specialization for high velocity (Table 2). Although much less dramatic than the
divergence of VM, VL obtains 1.5 times the
maximum excursion of RF and 1.4 times that
of VI. The fiber architecture of VL may indicate a compromise of force and velocity
within a single muscle (see Discussion).
The greater mass of VL is due not only to
a larger number of fibers, but also to the
presence of longer fasciculi which would increase its maximum velocity (i.e., excursion/
time). This is indicated by the ratio of wet
weight to predicted maximal tetanic tension
@%/PO),
which was calculated following Sacks
and Roy (1982) (Table 2). They used this parameter as a means of estimating the priority of force versus length-velocity for each
362
F.C. ANAPOL AND W.L. JUNGERS
hindlimb muscle in cat and interpreted high
ratios as indicating maximization of lengthvelocity. In the lemur, the highest (by nearly
threefold) value is seen in the parallel-fibered VM. Of interest is that the pinnatefibered muscle which monopolizes the force
output of the group (VL) also obtains a relatively high length-velocity priority. The values for RF and VI are equally low and
indicate priority of muscle force over lengthvelocity (for further discussion, see Sacks and
Roy, 1982).
The ratio of mean tendon length (tJ to the
mean fasciculus length plus G (i.e.,&t
tJ
is also presented in Table 2. Again, the parallel-fibered VM is distinct from the three
pinnate muscles. The two unipinnate mus-
+
cles (VI and VL) have similar values but both
are less than that of the bipinnate RF. Despite the fact that the fasciculi of VL are
continuous with tendon at both ends, when
compared to VI (in which the proximal end
of each fasciculus arises from bone), the
longer fasciculi in VL neutralize any expected increase over VI in this calculation.
Of the quadriceps, RF clearly has the
“longest” tendon per muscle fasciculus. Consequently, each fasciculus should expend less
energy (ATP hydrolysis) to transmit force to
bone than if its contractile tissue were to
extend the entire length of the muscle. VL
and VI have the second highest proportion
and although relatively close to RF’,the two
one-joint muscles are clearly different from
Fig. 7. Vastus medialis. A. ATPase preincubation at pH 10.35; B. ATPase preincubation at
pH 4.35; C. NADH-TR D. SDH. S, slow twitch-high oxidative fiber; FQ, fast twitch-high
oxidative fibers; F, fast twitch-low oxidative fiber.
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
RF. At the other end of the spectrum, VM
has the least amount of tendon per fasciculus.
Histochemistry
Light micrographs from cross sections of
VM, RF, VI, and VL are presented in Figures
7-10. In each group, four serial sections that
have been treated for myosin ATPase (preincubation at pH 10.35 and 4.4),NADH-TR,
and SDH have the corresponding cells in each
treatment labeled as to class. In VM,RF, and
VL, two cells have been identified as FOfrom each of the intermediate and darkstaining variety following treatment for alkaline myosin ATPase. These are thought to
correspond to the fast oxidative glycolytic
(FOG) and fast intermediate P i n t ) fibers in
the tetrapartite classification of fiber types
(Burke, 1975;McDonagh et al., 1980).
363
All three major cell classes, as well as all
three levels of alkaline myosin ATPase reactivity, are represented in VM, RF, and VL.
In VI, no F fibers are present and only slowand intermediate-staining fast fibers are observed. Also in VI, only fibers which stained
the darkest and intermediate levels for oxidative enzyme are present, as observed in
cells labeled S and FO in treatments for both
NADH-TR and SDH.
The means and ranges of fiber cross-sectional areas for each class of fibers are presented in Table 3 for individual animals. In
every muscle, fiber size is generally correlated to increasing reactivity of myosin ATPase and decreasing presence of oxidative
enzyme. Of interest is the extent to which
the ranges of some (but not all) classes
overlap.
Fig. 8. Rectus femoris (see Fig. 7 legend).
364
F.C. ANAPOL AND W.L. JUNGERS
Fig. 9. Vastus intermedius (see Fig. 7 legend).
In Table 3, the percentage of cross-sectional
area of each functional class of fiber type (S,
FO, F) is included for three lemurs. The
means and ranges of the three animals combined (composite lemur) are also indicated for
each class and depicted graphically in Figure
11.
A two-factorial analysis-of-variance table is
presented in Table 4. For S and F classes of
fibers, significant variability (P < .05) exists
among muscles but not among animals. Neither the overall variability among muscles
nor among animals is significant for the FO
class. In other words, the animals are similar
but the fiber-type properties of each muscle
are variable.
The Mann-Whitney U-test was employed
a s a nonparametric test of significant differ-
ences between all possible pairs of muscles
for each class of fibers (Table 5). For S fibers,
only VM and RF were not significantly different from one another (P < .05). For FO
fibers, VM and VI were not significantly different from one another, nor were RF and
VL. For F fibers, the only pairs not significantly different in their percentage of crosssectional area were RF and VL.
In all three animals, VI is the slowest and
most highly oxidative of the four muscles.
The most extreme example of this is observed in lemur 2, which is composed of 100%
S fibers. Of interest is the significantly higher
percentage of cross-sectional area occupied
by type S fibers in VL, when compared to
VM or RF. Although all three are predominated by fast fibers (FO plus F) VM has a
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
365
Fig. 10. Vastus lateralis (see Fig. 7 legend).
significantly smaller percentage of FO fibers with a higher concentration of fast, low-oxithan either RF or VL. VM is the fastest and dative fibers (F)toward midbelly.
the least oxidative of the four muscles, obDISCUSSION
taining the highest percentage of F fibers
The research design embodied in this work
and the lowest percentage of S.
In Table 6a, the relative fiber-type percent- presumes an association between specific
ages for VL in two lemurs (2 and 3) have physiological phenomena and the morphobeen partitioned into superficialldeep and logical features examined herein. Conseproximalldistal regions. For all three fiber quently, the interpretation of the results is
types, the disparity is greater between prox- subject to the “correctness” of these underimal and distal samples than between super- lying assumptions: (1)reduced physiological
ficial and deep. However, what is provided cross-sectional area and calculated maxihere is actually a progressive series of sam- mum excursion are taken as estimates of the
ples from proximal to distal and not a simple maximum effective force and maximum vesuperficialldeepdichotomy (Fig. 12,Table 6b). locity available to the animal from a muscle;
An appreciably higher concentration of (2) all but a negligible portion of the free
slower and more highly oxidative (S, FO) fi- elastic energy that contributes to the propulbers is found nearer to the attachment sites sive effort can be stored in the tendons rather
366
F.C. ANAPOL A N D W.L. JUNGERS
TABLE 3. Fiber-type percentage cross-sectional (cross-sec) area; fiber cross-sect. area'
Vastus medialis
No. 1(n = 187)
Mean fiber area (am')
Range (pm2)
% cross-sec. area
No. 2 (n = 402)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
No. 3 (n = 444)
Mean fiber area (pm2)
Range (pm2)
% cross-sec. area
Composite lemur (n = 1,033)
% cross-sec. area
Range (%)
Rectus femoris
No. 1(n = 210)
Mean fiber area (pm2)
Range (pm2)
% cross-sec. area
No. 2 (n = 178)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
No. 3 (n = 237)
Mean fiber area (pm2)
Range (prn')
% cross-sec. area
Composite lemur (n :
625)
% cross-sec. area
Range (%)
Vastus intermedius
No. 1(n = 145)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
No. 2 (n = 221)
Mean fiber area (pm')
Range (pm2)
% cross-sec. area
No. 3 (n = 299)
Mean fiber area (pm')
Range (pm')
% cross-sec. area
Composite lemur (n = 665)
% cross-sec. area
Range (%)
Vastus lateralis
No. 1(n = 323)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
No. 2 (n = 693)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
No. 3 (n = 670)
Mean fiber area (pm2)
Range (pm')
% cross-sec. area
Composite lemur (n = 1,686)
% cross-sec. area
Ranee (%)
I
S
FO
F
1.378
(94111,524)
1.6
2,082
(975-2,837)
32.9
3.357
(3,236-3,937)
65.5
1,813
(1,314-2,317)
1.4
3,016
(1,196-4,147)
15.6
4,895
(3,462-6,391)
83.0
1,182
(787-1,330)
0.9
2,225
(1,385-3,391)
18.6
3,209
(1,658-4,014)
80.5
1.3
(0.9-1.6)
22.4
(15.6-32.9)
76.3
(65.5-83.0)
2,115
0.5
4,816
(2,594-9,009)
39.4
6,361
(6,014-7,164)
60.1
2,531
(2,517-2,550)
5.4
4,178
(3,264-5,111)
28.6
6,950
(6,806-7,140)
66.0
1,994
(1,803-2,719)
5.5
3,141
(2,168-4,743)
29.1
4,148
(3.655-6.002)
65.5
3.8
(0.5-5.5)
32.4
(28.6-39.4)
63.8
(60.1-66.0)
2,841
(2,633-3,711)
75.2
3,687
(2,633-4,479)
24.8
0.0
2,210
(1,721-2,552)
100.0
-
-
0.0
0.0
2,948
(2,680-3,094)
71.9
3,482
(2,909-4,130)
28.1
0.0
0.0
0.0
82.4
(71.9-100.0)
17.6
(0.0-28.1)
0.0
2,020
(1,651-2,726)
13.8
2,180
(548-3,319)
28.7
4,151
(3,402-4,599)
57.5
2,123
(1,139-2,974)
8.6
3,969
(2,464-732)
21.8
5,657
(3,080-7,765)
69.7
1,794
(1,352-2,253)
5.2
3,124
(1,862-4,545)
37.0
3,575
(2,4354,655)
57.8
9.2
6.2-13.8)
29.2
(21.8-37.0)
61.7
(57.5-69.7)
-
0.0
0.0
-
IS, slow twitch - high oxidative; FO, fast twitch -high oxidative; F, fast twitch - low oxidative.
367
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
'r
than in the contractile machinery of the muscle fibers (Alexander, 1974; Alexander and
Bennett-Clark, 1977; but cf. Cavagna et al.,
1980); and (3) low and high myosin ATPase
activity are correlated to slow and fast rates
of tension development and increasing concentrations of oxidative enzyme reflect increasing resistance to "fatigue" (DennyBrown, 1929; Burke et al., 1971).
Electromyography of the quadriceps femoris in the locomotion and posture of Lemur fulvus is considered in detail elsewhere
(Jungers et al., 1980). In general, all four
muscles act synergistically to extend the crus
during normal locomotor behaviors. However, vastus intermedius assumes almost exclusive responsibility in maintaining tension
across the knee joint during posture. Because
the four muscles insert via a common tendon
closely applied to the anterior aspect of the
knee, differences in moment arms among
these muscles are presumed to be negligible.
Consequently, gross mechanical differences
related to leverage are virtually insignificant for the purposes of this analysis.
I
I
- -0
I
VASTUS LATERALIS
Fig. 11. Mean percentage of cross-sectional area for S,
FO, and F fibers in L. fuluus. Broken lines indicate range
for three animals.
TABLE 4. Twefactorial analysis of variance
(ANOVAfimuscles versus animals (no replication))'
Fiber Source of
type variation
S
FO
F
ANOVA
df
MS
SS
FS
A(musc1es) 3 7,739.31 2,579.77 2 9 . 46*
B(anima1s) 2
211.80
105.90 1 . 2 1 N S
Error
6
525.48
87.58
Total
11 8,476.59
A(musc1es) 3
346.33
115.44 1 . 77NS
B(anima1s) 2
401.47 200.74 3 . 08NS
Error
6
390.81
65.13
Total
11 1,138.61
A (muscles) 3 7,043.53 2,347.84 249. 77*
B(anima1s) 2
63.25
31.62 3 . 36NS
Error
6
56.40
9.4
Total
11 7,163.18
F,0512,3 =
5.14
F,0513,61=
Fig. 12. Intramuscular variation in vastus lateralis
(Lfuluus). Top-samples correspond to fiber-type percentages in Table 6a: 1,PxDp; 2, PxSu; 3, DsDp; 4, DsSu.
Bottom: Numbered sections include fasciculi that correspond to samples in top picture (see Results and Table
6b). Su, superficial; Dp, deep; Px, proximal; Ds, distal.
4.76
'NS, not significant; *Significant difference (d = ,051;df, degrees
of freedom; SS, sum of squares; MS, mean square; F,, sample
statistics of F distribution.
TABLE 5. Mann-Whitney U-test: all possiblepairs of muscles for each fiber type (a = .05)
S
Muscle
pair
VM x RF
VM x VI
VM x VL
RF x VI
RF x VL
VI x VL
ts
0.897
4.037
5.062
3.602
2.435
4.501
F
FO
Level of
significance
NS
.05
.05
.05
.05
.05
ts
Level of
significance
tS
Level of
significance
2.773
0.090
2.600
2.256
0.733
2.033
.05
NS
.05
.05
NS
.05
2.952
4.134
3.925
3.821
0.233
4.500
.05
.05
.05
.05
NS
.05
F.C. ANAPOL AND W.L. JUNGERS
368
TABLE 6. Intramuscular variation of fiber types in V L
for two lemurs (n = 1,363); Su: superficial; Dp: deep;
P x wroximalt Ds: distal: M: mean (see Fie. 12)
S
Su Dp M
a)
Px
Ds
M
Su
FO
Dp
M
Su
F
Dp
M
7.2 7.9 7.6 30.7 32.5 31.6 62.2 59.6 60.9
7.0 5.4 6.2 29.8 24.6 27.2 63.2 70.3 66.6
7.1 6.7
30.3 28.5
62.7 64.8
b)
PxDp (1)
PxSuQ)
DsDd3)
DsSu(4)
S
FO
F
7.9
7.2
5.4
7.0
32.5
30.7
24.6
29.8
59.6
62.2
70.3
63.2
TABLE Z Summary of morphological data for Lemur
fulvus-ratios; for each muscle, its derived value (see
Table 3) is divided by the lowest value o f the four
VM RF
If
4.7
Reduced physiological cross-sec. 1.0
area (% of group)
h
4.4
MassPo
4.5
1.0
ttflf + tt
Fiber types
(% cross-sec. area)
S
1.0
FO
1.3
F
1.2
VI
VL
1.0
3.6
1.1 1.5
2.6 10.1
1.0
1.0
2.6
1.1
1.1
2.4
1.5
1.5
2.4
2.9 63.4
1.8 1.0
1+
-
7.1
1.7
1.0
A profile for each muscle of the quadriceps
femoris in the brown lemur is presented below. The criteria upon which these profiles
are based are included only in the characterization of vastus medialis but are the same
for rectus femoris, v. intermedius, and v. lateralis. In order to facilitate comparisons
among muscles, parametric data are expressed as ratios in Table 7: for every parameter, the value of each muscle is divided by
the lowest of the fmr.
Vastus medialis
(1) Least potential effective tetanic force
(estimated by reduced physiological crosssectional area);
(2) highest potential velocity (estimated by
calculated maximum excursion and massPo);
(3) least potential conservation of energy
(estimated by length of tendon per fasciculus); and
(4)least time to maximum recruitment as
implied by a relatively high percentage crosssectional area of fast twitch, low oxidative (F)
muscle fibers.
Coupling long fasciculus excursion with a
preponderance of fibers that quickly rise to
peak tension, VM may be specialized to augment the most rapid or dynamic locomotor
activities with a late-onset surge of additional force. With a relative dearth of oxidative fibers, VM is poorly suited for sustained
contraction and, accordingly, would not need
to conserve energy (which is believed to be
required by “endurance-type” behaviors).
The low proportion of tendon per fasciculus
implies that this muscle is probably sacrificing some energy (that would otherwise be
conserved by transmitting force to bone
through noncontractile tendon) in favor of
increasing its potential velocity by the inclusion of contractile material along almost the
full length of the whole muscle.
The fast-fibered VM may be saved for more
strenuous activities which require rapid recruitment of additional muscle to augment
the propulsive effort. This would be compatible with current theory of motor-unit recruitment which hypothesizes that primarily Sand FO-type motor units are recruited for
activities as strenuous as fast running and
that F-type fibers are probably reserved for
more vigorous locomotor activities (Walmsley et al., 1978; Armstrong, 1980).
Rectus femoris
(1) Moderate potential effective tetanic
force;
(2) lowest potential velocity;
(3) highest potential conservation of energy; and
(4)low time to maximum recruitment with
high aerobic capacity.
The morphological features of RF suggest
that this muscle has the potential to sustain
either isometric or eccentric contraction during normal locomotion. Firstly, although RF
is the sole leg extensor to cross both the hip
and knee joints, its estimated maximal excursion is surprisingly small. Secondly, the
bipinnate arrangement of its muscle fibers
(contra Junders et al., 1980) allows a relatively high force output per gram of mass.
Thirdly, the high percentage of FO fibers
would allow muscle stiffening to occur almost instantaneously and repeatedly for extended periods of time.
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
Theoretically, RF could behave as a n elastic body, storing strain energy when stretched
during either hip extension andor knee flexion. This energy would be released when the
hip is flexed or the knee is extended. Not
only would coordination between the hip and
knee joints continually be maintained, but
the extensors of the thigh (e.g., femorococcygeus) could effectively contribute to leg extension through a stiffened, two-joint RF? Of
interest is that RF is recruited twice during
a single-step cycle, both as a n extensor of the
leg during support and again during swing
phase as it flexes the hip in order to recover
the limb for the next step cycle (Jungers et
al., 1980). A morphological configuration
which allows rapid development and continuous maintainance of isometric tension
seems well suited for a multifunctional muscle that flexes one joint and extends another.
369
percentage of highly oxidative fast-contracting fibers in a postural muscle would allow
a t least a portion of the muscle to keep pace
with the more rapidly contracting VM, RF,
and VL during relatively vigorous locomotor
activities such as galloping and leaping (a
constituative locomotor activity in lemur).
Vastus lateralis
(1)Highest potential effective tetanic force;
(2) second-highest potential velocity;
(3) relatively high potential conservation of
energy; and
(4)most heterogeneous distribution of fiber
types.
Among the quadriceps, VL is undoubtedly
the primary contributor to locomotion in L
fuluus. Its extraordinary mass includes statistically significant proportions of all three
classes of fibers, thereby broadening its range
of recruitment. This muscle, which obtains
Vastus intermedius
almost 60% of the combined mass of the
(1)Substantial potential effective tetanic group, appears to optimize a combination of
force, velocity, economy, and endurance.
force;
The architectural configuration observed in
(2) low potential velocity;
(3) relatively high potential conservation of V1 is especially suitable for leaping behavior.
Alezais (1900) and Stern (1971) concluded
energy; and
(4)longest time to maximum recruitment that the small proximal attachments of the
vasti peripherales in leaping rodents and priwith highest aerobic capacity.
VI is especially well suited for postural be- mates allow the muscle fibers to be longer
havior and is also recruited at high levels than those in nonleaping or climbing genera
during all progressive activities (Jungers et in which the corresponding attachments are
al., 1980). It is the deepest of the quadriceps, more extensive. In L. fuluus, a n exceptionwith muscle fibers arising directly from bone ally agile leaper, VM and VL both arise from
and passing close to the knee joint. All fea- circumscribed attachments at approximately
tures of its morphology suggest the ability to the same transverse plane at the proximal
maintain substantial isometric tension as end of the femur. Indeed, both are composed
well as slow, consistent, isotonic phasic activ- of relatively long fasciculi.
However, while the fibers of VM are parality for extensive periods of time. This is indicated by a population of entirely high- lel to the presumed line of action of the whole
oxidative muscle fibers, most of which ex- muscle, the fibers of VL are unipinnately
hibit myosin ATPase reactivity similar to arranged [in emendation of the long parallel
that known for slowly contracting fibers fibers previously described by Jungers et al.
(Denny-Brown, 1929; Henneman and Olson, (198011. The mean fasciculus length is slightly
1965; Burke et al., 1971; McDonagh et al., less than one-third of that for VM, despite
1980). This fiber-type composition is typical their similarity in whole muscle length.
With relatively long pinnate fibers, VL is
of demonstrably “postural” muscles, i.e, soleus (6.Smith et al., 1977; Walmsley et al., able to implement both high velocity and
1978; Burke, 1980; Smith et al., 1980; Gardi- considerable tension. Firstly, pinnation allows a n increase in the number of muscle
ner et al., 1982).
Substantial complements (24.8% and
28.1%) of FO fibers are present in VI in two
specimens (Table 3). This may reflect a n ex‘Cf. Walmsley et al. (1978).who suggested that the inherent
tended range of motor-unit recruitment in a n
stiffness in the fully active medial gastrocnemius in cat would
otherwise slow muscle (see Walmsley et al., transmit
forces from the powerful knee extensors to the
1978, for further discussion). A respectable calcaneus.
370
F.C. ANAPOL AND W.L. JUNGERS
fibers (i.e., the number of cross-bridges in
parallel) and, therefore, the amount of force
that can be applied to the tendon of insertion.
Secondly, the excursion of a pinnate whole
muscle is not merely proportional to but
longer than that of its constituent fibers (see
Gans, 1982; Muhl, 1982). Thirdly, because
they contain more sarcomeres in series, long
fibers (pinnate or parallel) are able to generate a n equivalent excursion with less shortening per sarcomere (Muhl, 1982). Consequently, longer fibers can maximize the
length-tension relationship by remaining
within a range of greater thirdthick filament
overlap (see Goslow et al., 1977; Walmsley
and Proske, 1981; Muhl, 1982). Because the
fasciculi of VL are considerably longer than
those of either RF or VI, it is the muscle best
suited for production of force and the pinnate
muscle best suited for velocity.
With a significant percentage of cross-sectional area composed of type S fibers, the
fiber-type distribution of VL is the most heterogeneous of the four muscles. Although
predominated by fast fibers (FO plus F) both
RF and VL are less specialized than VM with
its significantly higher percentage of F fibers. Because of their relative heterogeneity,
RF and VL would be expected to be active
over a wider range of locomotor activities
than either VM or VI.
Of additional interest is the distribution of
fiber types within VL. In extensor muscles,
the percentage of slow fibers is thought to
decrease from deep to superficial, presenting
a more-or-less-“stratified” arrangement
(Armstrong, 1980).This tenet could not apply
to unipinnate muscles (such as VL), whose
fibers are oriented superficial to deep, because the enzymatic activities within individual fibers are homogeneous throughout
their lengths (Pette et al., 1980). Alternatively, in VL both S and FO fiber types were
most highly concentrated near the joints (Table 6b). The fastest fibers with the lowest
oxidative enzyme levels were most highly
concentrated at midbelly. This is comparable
to results reported in lizard, in which FOG
and tonic fibers (sensu stricto) predominate
around joints in the hindlimb muscles with
FG fibers composing most of the overall muscle mass (Putnam et al. 1980).
Thus, the quadriceps femoris in L. fuZuus is
composed of four morphologically and (probably) functionally distinct muscles. Each is
characterized by a constellation of physiologically related architectural and histochemi-
cal features that underlies its particular
contribution to the propulsive effort. One
interpretation is that this broadens the range
of functional capabilities of the quadriceps as
a group. If in all of the four muscles the
architecturally related physiological alternatives (e.g., force versus velocity) were compromised, full realization of any parameter
would be limited for the entire group. However, the brown lemur retains three relatively specialized muscles: (1) VM-high
velocity at the expense of force and energy;
(2) RF-moderately high force and low energy cost a t the expense of velocity; and (3)
VI-a postural muscle. By contrast, there is
only a single ‘‘ comprehensive” muscle (VL).
One might suspect that the notably complex positional behavior of primates should
be associated with equally complex anatomical and physiological substrates. Studies of
primate locomotor behavior that tend to treat
species as if each were “specialized” for one
particular locomotor mode have been soundly
criticized by several workers (e.g., Stern and
Oxnard, 1973; Mittermeir and Fleagle, 1976;
Ripley, 1977) because this practice ignores
both the variation in complexity among locomotor “niches” (Stern and Oxnard, 1973)
and the requisite neurological and myological complexity in the animals, i.e., the dynamic input to complex locomotor behaviors.
Any hypothetical functional division of labor within lemur quadriceps may very well
be associated with a complex neuromuscular
requirement for rapidly traversing a threedimensional arboreal habitat. Although retaining the ability to move quite rapidly on
the ground with ease, the quadrupedal brown
lemur spends at least 90% of its time walking, running, and leaping through the upper
canopy levels of the forest (Walker, 1967;
Ward and Sussman, 1979; after Sussman,
1972).They (variably) prefer sloping and horizontal supports of large diameter and have
been observed to leap up to 4 m between
adjacent branch systems in lieu of continuous passages (Tattersall, 1982).
When compared to other mammals (e.g.,
cats), lemurs appear to be relatively flexible
with respect to neural programming of interlimb coordination (Jungers and Anapol,
1985);i.e., a single motor “program” will not
suffice for all gaits. This implies that lemurs
rely more upon facultative peripheral input
to modulate their neuromuscular outputs.
The anatomical substrates of their locomotor
behavior would therefore be expected to sub-
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
serve and reflect this requisite flexibility. In
essence, the great complexity of an arboreal
habitat (e.g., variability among substrate diameters and juxtaposition of trees and
branches) probably requires exceptional precision with respect to control of the locomotor
apparatus; the neuromuscular system must
be able to provide rapid adaptability to a
grossly irregular and often precarious arboreal topography.
The expression of the standard deviation
as a percentage of the mean of the population
can be used to compare populations of appreciably differing means (Sokal and Rohlf,
1981). Thus, the morphological diversity
among VM, RF, VI, and VL was further illustrated by calculating the coefficient of variation adjusted for small sample bias (V*) for
each parameter in this study (Table 8). The
V* values indicate that for most of these
parameters, all muscles vary considerably
about the mean of the four.
Of all the parameters included in Table 8,
the percentage cross-sectional area of FO fibers has the lowest coefficient of variation
among muscles. This class includes a wider
variety of cells than either the S or F classes.
It includes cells of both intermediate and
high myosin-ATPase reactivity, the former
having been correlated to slightly slower
speeds of contraction (Burke, 1981). Fast
twitch-high oxidative fibers also include two
levels (dark and medium) of concentration of
oxidative enzymes, thereby providing additional variety in aerobic capabilities (socalled “resistance to fatigue”).
The range of cross-sectional areas of FO
fibers is also considerably broader than that
of either S or F classes (Table 3). In addition,
among the three classes of motor units in cat
gastrocnemius, the FO units have the fewest
muscle fibers per axon (Burke and Tsairis,
1973). If this relationship holds for lemurs,
TABLE 8. Coefficients of uariation’
Parameter
lf
Reduced physiological cross-see.area
h
MassPo
ttfif
+ tt
Fiber types
S
FO
F
v* * s*,
89.5
98.1
85.4
85.7
37.9
k 31.6
k 34.7
+ 30.2
k 30.3
k 13.4
171.2 k 60.5
27.9 k 9.9
72.1 25.5
+
‘V*, coefficient of variation corrected for small sample size: sV*,
standard error of the statistic.
371
the FO portion of cross-sectional area could
be recruited in variably smaller parcels than
either the F or S units.
Despite the occurrence of dramatic architectural differences among the four heads of
the quadriceps in the brown lemur, a means
is provided by which the different potentials
within and among muscles can be realized to
produce a smooth and more-or-less-continuous power band. In other words, while disparate architectural profiles expand the range
of functional capabilities for the quadriceps
as a group, physiological continuity is maintained among muscles by the presence of substantial pools of an intermediate, relatively
heterogeneous class of fibers that serves as a
“common denominator.”
Other mammals whose habitats appear to
require flexible circuitry for neuromuscular
control also exhibit a relatively balanced fiber population. For example, observations of
Tupaia glis indicate that this species is both
arboreal and terrestrial. However, the arborealherrestrial dichotomy may be artificial
for an animal this size because the relatively
cluttered forest floor offers the same impediments to locomotory progression as encountered in the trees (Jenkins, 1974). Thus, the
locomotor repertoire of tree shrews is adaptive to “two major topographical features”
which favor a “highly flexible and versatile
locomotor pattern”: (1) surfaces that are not
level, and (2) a spatial arrangement of locomotor surfaces that is disordered (Jenkins,
1974, pp. 110-111).
The critical factors linking lemur and tree
shrew locomotor behavior are (1)their habitual exploitation of a three-dimensional environment regardless of the extent to which it
is “arboreal” or “terrestrial”, and (2) such
exploitation often executed at high velocities
(as in running, galloping, or leaping). The
quadriceps in both lemur and tree shrew are
composed of relatively heterogeneous (no category less than 20%) distributions of fiber
types, which includes a large percentage of
FO fibers (Table 9).
The association between the behavioral and
histochemical features characteristic of the
lemur and tree shrew can be contrasted to
that for cat (Felis domesticus), dog (Canis
familiaris), loris (Nycticebus coucang), and
lesser bushbaby (Galago senegalensis). For
these taxa, percentages (unadjusted for crosssectional area) of three major classes of fibers
in quadriceps femoris are presented in Table
9.
372
F.C. ANAPOL AND W.L. JUNGERS
TABLE 9. Fiber-type percentages in quadriceps femoris for various
species (decreasing quantities of S fibers)
Loris (Sickles and Pinkstaff, 1981)
VM
RF
VI
VL
Mean quadriceps femoris
Dog (Armstrong e t al., 1982)
VM
RF
VI
VL
Mean quadriceps femoris
Cat (Ariano e t al., 1973)
VM
RF
VI
VL
Mean quadriceps femoris
Lemur (Anapol, 1984)
VM
RF
VI
VL
Mean quadriceps femoris
Tree shrew (Sickles and Pinkstaff, 1981)
VM
RF
VI
VL
Mean quadriceps femoris
Lesser bushbaby (Sickles and Pinkstaff,l981)
VM
RF
VI
VL
Mean quadriceps femoris
Cats and dogs are the most cursorially
adapted of the carnivores (Howell, 1944).Felids, in general, are best characterized by a
“prey-capture” mode of behavior (Eisenberg,
1981). In domestic cats this entails (1)a fast
run in a crouched position or slow stalking of
prey, and (2) springing onto prey during
which the cat “darts forward flattened
against the ground, either running or with
several bounds” (Leyhausen, 1979, p. 6; also
see Gambarayan, 1974). They usually do not
chase their prey among the branches nor
among the trees, and their large size effectively eliminates a considerable portion of
the impediments to locomotion (such as uneven terrain) that faces animals the size of
tree shrews. The fiber-type distribution in
quadriceps femoris in cats is relatively polar-
s
PO
64
55
86
52
64
36
45
14
48
36
-
39
41
88
43
53
61
59
12
57
47
-
13
22
98
27
40
18
69
61
3
8
85
15
28
27
38
15
33
29
70
54
52
44
1
10
92
75
57
25
32
8
-
4
27
72
53
23
20
1
3
49
24
45
51
14
34
75
52
86
53
-
13
~
17
2
17
14
F
-
-
-
-
56
47
ized (Table 9). Preferential selection of slow
and fast-low oxidative fibers (at the expense
of FO) would seem to be adaptive for both
their stalking behavior (which is executed in
poised position, regardless of speed) and
springing (pouncing) behavior, respectively.
By contrast, dogs pursue prey terrestrially
for relatively long distances at moderate running speeds (Howell, 1944; Gambarayan,
1974; Eisenberg, 1981). Of no surprise is the
exclusive occurrence of highly oxidative fibers (S; FO) in all of their hindlimb muscles
(Armstrong et al., 1982). Dogs (and loris) lack
F fibers and have the least-heterogeneous
fiber-type distributions of the animals presented here. They both exhibit fiber profiles
which emphasize slower contraction and high
endurance.
ARCHITECTURE AND HISTOCHEMISTRY IN LEMUR QUADRICEPS FEMORIS
The slow climbing of Nycticebus coucang
(Walker, 1967) presents a relatively less precarious locomotory situation for this arboreal
quadruped. With usually two or three feet
grasping the support (Walker, 1967; Dykyj,
1980), the need for rapid adjustment to the
variety of substrates found among the trees
is dramatically reduced. Constituent fiber
types in loris are exclusively the high-endurance variety, most of which are slow contracting (Sickles and Pinkstaff, 1981).
Electromyography has indicated that some
leg muscles remain active for longer periods
of time in slow loris than in more rapidly
moving animals covering the same distance
(see Anapol and Jungers, 1982; Jungers et
al., 1983).
At the other extreme (relatively few S fibers) is Galago senegalensis. Lesser busbabies are primarily tree dwellers that leap
among branches with great agility, although
a t slower speeds they have been observed to
move quadrupedally and have also been observed “waddling” quadrupedally on the
ground (Walker, 1967). Among the four arboreal (or semiarboreal, in the case of tree
shrews) species presented in Table 9, increasing populations of faster and less oxidative
fibers (loris < tree shrew < lemur < bushbaby) are correlated with a n increasing proclivity for leaping a s a primary mode of
locomotion (see Gillespie et al., 1974; Sickles
and Pinkstaff, 1981); for example, leaping is
a much-higher-frequency mode in Galago
than in L fulvus (Walker, 1967; after Attenborough, 1961). Moreover, results from in
vivo mechanical studies of hindlimb muscle
function in G. senegalensis predict the presence of a high proportion of fast twitch-low
oxidative fibers in the quadriceps femoris
(Hall-Craggs, 1974).
The results presented here encourage speculation regarding expected intramuscular
morphological configurations in other primates. Great architectural disparity among
synergists coupled with overall fiber type
heterogeneity (including a substantial proportion of fast twitch-high oxidative fibers)
is the likely set of character states in animals
whose locomotor repertoires require rapid
adaptability to complex substrates. Among
anthropoid primates, this would include
those taxa which exploit arboreal environments with rapid quadrupedalism and leaping among trees and branches, e.g., Saimiri
or Aotus (Fleagle and Mittermeier, 1980;
373
Plaghki et al., 1981) and leaf monkeys such
as Presbytis melalophos (Fleagle, 1977).
Alternatively, hindlimb muscles in primates committed to locomotor modes less dependent upon such flexibility, e.g., Erythrocebus (terrestrial quadrupedalism), Tarsius (obligatory leaping), or Homo (bipedality), would exhibit less architectural diversity
and more polarization of fiber types (predominantly slow and fast twitch-low oxidative
fibers). Species whose locomotor repertoires
habitually include more than a single locomotor mode, e.g., L catta, which spends considerably more of its time on the ground than
other lemur species (Walker, 1967; after Jolly,
1966; Ward and Sussman, 19791, present different possibilities. For example, would the
muscle morphology of these forms adhere to
a model that emphasizes their most frequent
behavior mode or one that lies somewhere
between the extremes described above?
Nevertheless, the results reported herein
support the hypothesis that the behavior of
a n animal is associated intimately with the
architectural and histochemical bases of its
anatomy. Whether the interpretation of these
results can be extended without modification
to other vertebrate groups and to other musculoskeletal systems in general remains to
be tested.
ACKNOWLEDGMENTS
We wish to express our sincere appreciation to David S. Carlson, Maynard M. Dewey,
John G. Fleagle, Susan W. Herring, Farish
A. Jenkins, Jr., Jack T. Stern, Jr., and anonymous reviewers for their invaluable comments and criticisms on the manuscript. A
special thank you to Luci Betti for preparing
the expert graphs and illustrations, and to
George Boykin, Norman Creel, Steve Hartman, Eileen Schneider, and Robert Skinner
for their technical advice and assistance.
Financial support was provided by the Department of Anatomical Sciences, State University of New York a t Stony Brook, NIH
biomedical
research
grant
BSRG
2SO7RRO573610 to W.L. Jungers, and NSF
research grant BNS 8119664 to J . T. Stern,
Jr., W.L. Jungers, and R.L. Susman.
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