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An electromyographic study of serratus anterior in atelines and Alouatta Implications for hominoid evolution.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 52323-334
(
19801
An Electromyographic Study of Serratus Anterior in
Atelines and Alouatta: Implications for Hominoid Evolution
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, AND
ANDREA K. VANGOR
Department of Amtomical Sciences. Hecrlth Sciences Center, State Uniuerszty of
New York at Stony Brook, Long Island, N e w York 1 1 7Y4 (J.T.S., W.L.J., and
A . K . V . )and West Virginia School of Osteopcrthic Medicine, Lewishurg, West
V i r g h i a 24901 1J.P.W.)
K E Y WORDS E l e c t r o m y o g r a p h y , H o m i n o i d
evolution, Serratus anterior, New World monkeys
ABSTRACT
The serratus anterior pars caudalis muscle of nonhuman primates displays anatomical differences among genera that can be attributed to
differences in the mechanical demands placed on these genera by their diverse
locomotor behaviors. In primates that engage extensively in climbing and suspensory behaviors, the caudal digitations of this fan-shaped muscle are aligned more
nearly parallel to the long axis of the trunk. In order to clarify the selective factors
promoting such a morphological change, we have conducted a telemetered electromyographic study of the caudal and middle digitations of the serratus anterior pars
caudalis. During voluntary elevation of the forelimb, only the middle, more
obliquely disposed digitations are powerfully recruited. The caudal digitations are
either inactive or functionjust to initiate scapular rotation. During locomotion, the
middle digitations act in the swing (recovery)phase, whereas the caudal digitations are predominantly active in the support (propulsive) phase. These findings
suggest that the caudal digitations are important in propelling the trunk past the
scapula during locomotion. Evolution of a fiber orientation more parallel to the
long axis of the trunk is suggested to have occurred in broad chested primates for
the purpose of facilitating locomotor behaviors requiring caudal scapular retraction for propulsion, but which would be deleteriously affected if such retraction
were linked to simultaneous ventral displacement of the shoulder girdle. In its
current state, the human serratus anterior seems clearly adapted for arm-raising
functions and indicates descent from a small ape with a thoracic shape similar to
atelines.
The serratus anterior pars caudalis muscle of
nonhuman primates has been shown to display
anatomical differences among genera that can
be attributed to differences in the mechanical
demands placed on these genera by their diverse locomotor behaviors. The muscle is fanshaped in all primates, consisting of a number
of digitations arising from the outer surfaces of
ribs and converging to an insertion on the inferior angle of the scapula (Fig. 1).Ashton and
Oxnard ('63) reported that if anthropoid primates are categorized as either quadrupeds,
semibrachiators, or brachiators, there occurs
a n increase in the number, length, and thickness of digitations in this series of locomotor
groups. Additionally, the rib bearing the most
caudal digitation is commonly the ninth in
quadrupeds, tenth in semibrachiators, and
0002-9483/80/5203-0323$02,30 ((3 1980 ALAN R. LISS, INC.
eleventh in brachiators. Ashton and Oxnard
interpreted the increase in thickness and
weight of the serratus anterior pars caudalis in
brachiators, and to a lesser degree in semibrachiators, as being an adaptation to facilitate
the rotation of the scapula occurring in armraising. They further noted that during suspension, the thick caudal digitations will be
almost vertical and can transmit weight from
the lower part of the trunk to the scapula. These
conclusions formed the basis for selecting measurements to reflect the rotary moment arm of
the serratus anterior on the shape of the scapula in nonhuman primates in subsequent publications (Ashton and Oxnard, '64; Ashton et
al., '65; Oxnard, '67).
Received April 20, 1 9 7 9 accepted Auwust 17. 1979
323
324
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, A N D ANDREA K. VANGOR
,
HOWLING
MONKEY
Jf
MONKEY
Fig. 1. A comparison of the structure of the serratus anterior between the spider monkey {Ateies) and the
howling monkey iAlouattal. Note that although the muscle attaches to the same ribs in both genera, the most
caudal digitations are oriented more parallel to the long axis of the trunk in the spider monkey. This difference is a
result of the greater obliquity of the ribs in Ateles and of the more dorsal site of muscular attachment to the outer
surfaces of the lower ribs in this genus.
In order to determine whether or not the
morphological specializations of the serratus
anterior pars caudalis in “brachiators” and
“semibrachiators” could be attributed to a special role of this muscle in arm-raising or suspension, Stern, et al. (’77)conducted a telemetered electromyographic study of this muscle in
one individual ofAteles fusciceps ( d)and one of
Lugothrix lugothrichu ( 0 1. These authors report that in Ateles, the muscle is much more
active in the support (propulsive)phase of armswinging and vertical climbing than in the
swing (recovery) phase, suggesting a major role
in propulsion by pulling the trunk up a t the
scapulothoracic joint, and a minor role in armraising. In the woolly monkey, the activity during arm-raising was relatively greater. This
observation was interpreted by postulating
that the act of raising the arm requires more
extensive scapular rotation in the woolly monkey because it has a less cranially directed
glenoid fossa.
Tuttle and Basmajian (’77, ’78) report the
results of experiments on the caudal portion of
the serratus anterior inPongo, Pun troglodytes,
and Pan gorilla. They note variable EMG activity during arm-raising, such a movement
often being accompanied by only low potentials
EMG OF SERRATUS ANTERIOR
or electrical silence. High activity, when it occurs, is generally confined to the beginning of
movement. During hoisting behavior and
quadrupedal walking, the muscle was either
silent or active a t a low level. Pendant suspension did not recruit the caudal portion of serratus anterior. Tuttle and Basmajian interpret
the relatively slight activity of the serratus anterior during armswinging by great apes as
correlated with their cranially directed glenoid
fossae and consequently diminished need for
scapular rotation.
The difficulty with drawing conclusions from
existing data about the role of the serratus anterior in the locomotion of nonhuman primates
is that neither of the published studies has
specified in any detail the location of the electrodes. This takes on special importance for
studies of the serratus anterior because it is a
broad fan-shaped muscle with independent
digitations (Fig. 1 ) that need not function together.
In order to examine the possibility that the
different digitations of the serratus anterior
play fundamentally different roles in locomotion, we have undertaken a more exhaustive
telemetered electromyographic study of this
muscle in the spider monkey (Atelesl, t h e
woolly monkey (Lagothrixi, and the howling
monkey (Alouattaj.
325
1 Cercopithecus aethiops, 1Cebus nigriuitatus,
1Chiropotes satanas, 1 Alouatta seniculus, 1A .
caraya, 1 A . palliata, 2 Lagothrix lagothricha, 1
Ateles paniscus, 1 A . geoffroyi, 1A . fusciceps, 2
Hylohates lar, 1 H . syndactylus, 1 Pongo pygmaeus, 1Pan troglodytes, and 7 f f o m osapiens.
Methods
We employed the technique of telemetered
electromyography described by Stern e t al. (’77)
as modified by Stern et al. (’80).This technique
permits the subjects to move freely and naturally without hindrance of wires running from
the animal to a recording device. It also allows
quantification of the relative amplitude of
EMG activity.
Electrode placement
The individual digitations of the serratus anterior cannot be palpated in the subject animals, and we were constrained to rely on bony
landmarks to guide insertion of electrodes. Attempts were made to place separate electrodes
in one of the caudal digitations and one of the
middle digitations of the muscle. For the
former, we palpated the rib that lies deep to the
intersection of the posterior axillary line with a
transverse plane a t the level ofthe xiphisternal
joint. The needle carrying the electrode pair
was inserted a t this intersection until the rib
was contacted. Then the needle was directed
MATERIALS AND MEI’HOUS
dorsally along the surface of the rib for apExperimental Subjects
proximately 1 cm. In order to impale a middle
The subjects for the electromyographic ex- digitation of serratus anterior, we palpated the
periments were 2 spider monkeys, ( 1d A . fus- rib that lay deep to the intersection of the midciceps and 19 A. helzebuthi, 2 woolly monkeys axillary line with a transverse plane half way
(1d a n d 1 0 L . lagothricha), and 1 howling between the jugular notch and xiphisternal
monkey ( 9 A. seniculus). All subjects were joint. The insertion of the needle was as deadults (the howling monkey rather aged) show- scribed for a caudal digitation.
In most instances, the serratus anterior was
ing no obvious pathology. They had been
housed in a large enclosure (7.3 m x 3.7 m studied simultaneously with the latissimus
x 2.7 m) for a t least 6 months prior to study. dorsi and external abdominal oblique in order
Within the enclosure were a long horizontal to verify that electrodes in the serratus were
tree trunk (7.3 m x 9.5 cm), placed approxi- not detecting activity in these other muscles.
Our method of inserting electrodes by no
mately 60 cm above the ground, a long vertical
tree trunk (3.7 m x 8.5 cm), and a 7.3 m long means guaranteed that the same digitation
ladder, with wooden dowel cross pieces (2.8 cm would be impaled on every attempt that was
diameter) spaced 40 cm apart, suspended from made. Records from what we have designated
the roof of the cage. The subjects were accus- as a “caudal digitation” probably are sampling
tomed to moving on these supports and were fibers arising from ribs 7 or 8. Our “middle
digitation” probably corresponds to fibers arisenticed to do so with rewards of food.
ing from rib 5 . However, it is possible that in
Anatomical specimens
any given experiment we may have missed the
Although the primary focus of this study is mark by one rib level up or down. For this
not anatomical, we did attempt to confirm the reason, we shall concentrate our presentation
findings of Ashton and Oxnard (’63)by dissect- of results on experiments in which a caudal and
ing the serratus anterior of the following spec- middle digitation were studied simultaneously.
imens: 1Erythrocehus patas, 1 Macaca mulatta, In these cases there was almost certainly a gap
326
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, AND ANDREA K. VANGOR
of at least one rib between the origins of the
sampled fibers. The total number of experiments contributing to our analysis are as follows: four on a caudal digitation in Ateles, six
on a middle digitation indteles, two on a caudal
digitation in Lagothrix, two on a middle digitation in Lagothrix, one on a caudal digitation in
Alouatta, and one on a middle digitation of
Alouatta.
RESULTS
Anatomical
Since we did not conduct a thorough comparative anatomical study on large samples of
nonhuman primates, we wish to confine discussion of our anatomical findings to one issue that
will be of relevance for interpretation of the
electromyographic result,+i.e., the origin and
orientation of the most caudal fibers. Our anatomical data (Table l )suggest that although a
valid relationship between locomotor behavior
and the most caudal rib of origin might emerge
when primates are grouped as quadrupeds,
semibrachiators, and brachiators, such a relationship does not appear as clearly when individual genera are considered, and it is further
confounded by substantial intrageneric
morphological variation (Kohlbrugge, 1897).A
more important observation, we think, is that
the angle made by the most caudal digitation
with the long axis of the trunk is largely independent of the number of the rib from which
it arises, but instead is closely tied to the
obliquity of the ribs and the specific site of attachment to them'.
Figure 1 demonstrates that the caudal digitations of serratus anterior are aligned more
nearly parallel to the craniocaudal axis in
Ateles than inAlouatta, even though the slips of
muscle arise from the same ribs in both genera.
The basis for the difference in orientation is the
greater obliquity of the ribs in Ateles and the
fact that the origin of the muscle is located more
dorsally on the outer surface of the ribs. Such
traits also characterizeHylohates. They are ex-
aggerated in Pongo and Pan troglodytes so that
the caudal edge of serratus anterior in these
great apes makes an angle of only 1C15"with
the long axis of the trunk.
Electromyographic
Voluntary movements
A clear functional distinction between the
caudal and middle digitations of serratus anterior is indicated by their electrical activities
during voluntary reaching movements involving either protraction or abduction of the arm.
Figures 2-5 illustrate the activities of the
caudal and middle digitations of the serratus
anterior in Ateles and Lagothrix during examples of reaching that presumably entail rotation of the scapula to direct the glenoid cavity
more cranially. It can be seen that, a t most, the
caudal digitation of the muscle is active only to
initiate the rotatory movement. Activity in the
caudal digitation is quickly superseded by a
powerful contraction in the middle digitation to
continue scapular rotation and to hold the position. In some instances, during which the caudal digitation exhibited a low level of postural
activity prior to the intiation of the reach, its
activity was actually terminated as the limb
began its movement.
Locomotion
The behavior of climbing the vertical trunk
elicits high levels of activity in the serratus
anterior, and the phasic recruitment during
this behavior demonstrates the functional distinction between the middle and caudal digitations.
Figure 6 illustrates the phasic activities of
middle, "intermediate," and caudal digitations
of the serratus anterior as revealed in three
separate experiments on 2 specimens of Ateles.
Data for the middle and caudal digitation of
'We have discussed th is ohsewation with Charles Oxnard, who
agrees th a t I t more nearly reflects his own findings. The use of rih
numbers in Ashton and Oxnard 1'63)was an a tte mp t to quantify these
findings.
T A B L E 1. Rih from which most caudal digitation o f serratus anterior arises
in a small sample of anthropoid primates
Rib 8
E . patas
C. aethiops
C. satonas
A . caraya
A . polliato
L . lagothricha
H . sapiens
Rib 9
Rib 10
A . seniculus
A . paniscus
A. geoffro,yi
H . sapiens
M . mulatto
C . nigriuztatus
A . fusciceps
H . lar
H . syndactylus '
P. pygmaeus
P. paniscus'
'Kohlhrugge 1 lH90l
'Miller 1'52)
'Primrose 11898-1899). S te wa r t 1'36)
'Stew;rrt 1'36)
'Raven 1'50)
Rib 11
Hylobates species'
H . lar
H . syndactylus
P. pygmaeus '
P. troglodytes'
Rib 12
P. troglodytes
P. gorilla4
Rib 13
P. gorilla'
327
EMG OF SERRATUS ANTERIOR
n
SERRATUS
ANTERIOR
MIDDLE
DIGITATION
SERRATUS
ANTERIOR
CAUDAL
DIG1 TAT I 0 N
EXTERNAL
ABDOMINAL
OBLIQUE
I
I
Fig. 2. Electromyopaphic activity of the right serratus anterior during a n upward reach by a woolly monkey.
At the start of the EMG traces, the upper limb is already elevated to reach for food. Both middle and caudal
digitations of the serratus anterior are active. A t the moment marked by the first vertical dotted line, the animal
makes a n extreme reaching effort. The caudal digitation ceases to fire and the rotatory movement of the scapula
relies on a very powerful contraction of the middle digitation. The arm is then returned to a lower position (last
vertical dotted line) and slight scapular rotation is maintained in this posture by the caudal digitation ofserratus
anterior.
LATISSIMUS
DORSI
-
SERRATUS
ANTERIOR
MIDDLE
DIG I TAT1ON
SERRATUS
ANTERIOR
CAUDAL
Dl GITAT I 0N
EXTERNAL
ABDOMINAL
OBLIQUE
Fig. 3 . Electromyographic activity of the right serratus anterior during a forward and upward reach by a
spider monkey i n a pronograde posture supported by hindlimbs and tail. The initial scapular rotation is effected by
the caudal digitation, but activity in this muscle bundle soon ceases and is supplanted by powerful recruitment of
the middle digitation to complete the movement.
328
y$
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS,
AND
ANDREA K. VANGOR
LAT ISSIMUS
DORSl
SERRATUS
ANTERIOR
MIDDLE
DIG I TAT1 ON
SERRAT U S
ANTE RI OR
CAUDAL
D IGITAT I0 N
II .1
11
I'
I
'
.
1
EXTERNAL
OBLIQUE
Fig. 4. Electromyographic activity of the right serratus anterior during a n upward reach by a spider monkey
standing bipedally. The caudal digitation is virtually silent both in maintenance of the partially elevated posture
of the upper limh and in the reaching effort.
L A T IS S I M US
DORSl
SE R R A T U S
ANTERIOR
MIDDLE
D I GI TAT I 0 N
SERRAT US
ANTERIOR
CAUDAL
DIGITATION
3
EXTERNAL
ABDOMINAL
OBLIQUE
4:
Fig. 5 . Electromyographic activity of the right serratus anterior during a downward reach by a spider monkey
hanging by its tail. Both digitations of the serratus anterior are active to maintain the posture of the upper limh
against the downward pull of gravity. However, upon executing a reach requiring scapular rotation, the caudal
digitation ceases to fire and the middle digitation is powerfully recruited.
329
EMG OF SERRATUS ANTERIOR
MjDDLE DIGITATION
animal I
I
I
I
1
\ B SUPPORT
A (81
i
I
1
INTERMEDIATE
DIGITATION
I
I
SWING (11)
I
!
I
I
S W I N G (41
SLPPORT ( 6
I
CAUDAL DIGITATION
animal I
1
J
,
n n A b A
'
SUPPORT (8)
1
SWING ( 1 1 )
C A U D A L DIGITATION
animal 2
I
I
I
I
I
SUPPORT ( 9 )
SWING (12)
Fig. 6. Phasic activity patterns of a middle, intermediate, and caudal digitation of the serratus anterior in one
spider monkey ( A .fiscictepsd-animal I), and of a caudal digitation in a second spider monkey ( A . beizebuth
animal 2 ) ,during climbing a vertical trunk, Blackened areas represent activity occurring more than 75% of the
time. White enclosed areas represent activity occurring more tkan 50%, but less than 75% of the time. The height
of the left margin of the support phase indicates maximum observed activity. In parentheses following the words
SUPPORT and SWING a r e the number of step cycles digitized (Sternet al., '80) to produce this figure.
It can be seen that the middle digitation acts predominantly during the swing phase, presumably to produce the
scapular rotation that accompanies recovery of the upper limb to grasp a new and higher hold on the trunk. Its
activity was virtually identical in both specimens ofilteles. The caudal digitation acts in the opposite part of the
cycle. It appears to be propulsive in nature pulling the trunk up through the scapula. The intermediate digitation
was so designated because its activity pattern was found to be intermediate to the other two.
The variation between subjects in the activity of the caudal digitation is considerable. In animal 2, the greatest
effort of these fibers occurs at the end of the pull-up, whereas it occupies the first :% of this phase in animal 1.It is
even possible t h a t the activity in animal 2 just prior to release of grasp is related to the initiation of the scapular
rotation of swing phase.
0-
animal 1 (A.fusciceps d ) are derived from the
same experiment. A second experiment, attempting to sample a middle digitation of
the same subject, yielded results indicating a
pattern o f recruitment almost perfectly intermediate between the digitations of the first
experiment. We are of the opinion that these
results represent the true phasic activity of a
digitation anatomically intermediate between
what we have called mjddle and caudal. Also
included in Figure 6 is a representation of the
phasic activity of a caudal digitation of animal
2 ( A .belzebuth 9). The middle digitation of this
specimen was recruited identically to that of
330
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, AND ANDREA K. VANGOR
animal 1,but the behavior of the caudal digitation indicates a noteworthy degree of intrageneric variation.
Figure 6 shows very clearly that just as the
middle digitation is recruited powerfully for
voluntary elevation of the arm, so i t is powerfully employed in the swing phase of vertical
climbing. The caudal digitation is silent during
the major portion of swing phase, as would be
expected from its similar inactivity in voluntary elevation of the arm. The high levels of
activity of the caudal digitation during the
support phase of vertical climbing point to a
role for this portion of the muscle in propulsion.
In other words, the trunk is pulled up through
the scapula as part of the effort of climbing.
Although the caudal digitation acts predominantly during support phase in both specimens
of spider monkey, i t can be seen from Figure 6
that the variation between these animals is
consjderable. In animal 2, the greatest effort of
the caudal digitation is a t the end of the
pull-up, whereas it occupies the first 34 of this
phase in animal 1. It is even possible that the
activity in animal 2 just prior to release of
grasp is related to the initiation of the scapular
rotation of swing phase.
Figure 7 illustrates the activity of the middle
and caudal digitations of the serratus anterior
of a woolly monkey during climbing a vertical
trunk. Again the distinct role of the middle
digitation for elevation of the arm and that of
the caudal digitation for propulsion are evident. However, unlike the case of the spider
monkey, all our experiments on caudal digitations in the woolly monkey show activity a t the
onset of swing. The most likely explanation for
this observation is that the caudal digitations
in the woolly monkey are not as vertically
aligned as in the spider monkey and, therefore,
possess a rotatory function that is impossible
for a digitation attaching to the same rib in
Ateles.
The separate locomotor roles of the digitations of serratus anterior are further illustrated by their recruitment patterns in armswinging (Fig. 8). The 2 specimens of spider
monkey exhibited virtually identical patterns
of muscular activity. The middle digitation
serves the function of scapular rotation during
the swing phase of the cycle whereas the caudal
digitation acts during the support phase. As
pointed out by Stern et al. ('77)this latter activity correlates well with the finding by Jenkins et al. ('78) that caudal retraction of the
scapula is an important element of scapulothoracic movement during armswinging in
Ateles.
We were unable to elicit pendular armswinging in the woolly monkey frequently enough to
gather meaningful data'. However, the phasic
activity pattern in another kind of suspensory
behavior, suspended quadrupedalism, shows
the rotatory role of the middle digitation in
contrast to the propulsive role of the caudal
digitation (Fig. 9).
Finally, Figure 10 illustrates the activities of
the caudal digitation of the serratus anterior of
Alouatta seniculus during pronograde quadrupedalism along a horizontal trunk. The distinction between rotatory and propulsive functions
is clear. A similar distinction occurs also in
woolly and spider monkeys during pronograde
quadrupedalism. However, in the atelines, and
especially so in the spider monkey, the support
phase activity of the caudal digitation is often
accompanied by recruitment of the middle digitation. It is possible that the serratus anterior
pars caudalis can assist that muscle's cranial
part in preventing dorsal displacement of the
vertebral border of the scapula during the support phase of quadrupedalism. On the other
hand, the increasing recruitment of the middle
digitations during support phase from howling
to woolly to spider monkey correlates with the
increasing craniocaudal orientation of these fibers, and suggests that they may have a propulsive role in quadrupedalism in atelines.
DISCUSSION
All the data we have gathered clearly point to
a major functional distinction between the
middle and caudal digitations of the serratus
anterior of prehensile-tailed cebids. This finding is not affected by the most obvious weakness in our study, the inability to ascertain
with certainty the exact digitation into which
the electrodes were placed. The data presented
here (with the exception of that for suspended
quadrupedalism in Lagothrix) all represent
comparisons between middle and caudal digitations sampled simultaneously. Therefore,
even if we cannot precisely determine the function of a particular digitation, we can assert
definitively that the more caudal digitations
differ from the more cranial ones in being increasingly propulsive and less rotatory in function.
The data presented clarify the findings of
Stern et al. ('77)and Tuttle and Basmajian ('77,
'78). The former suggest that the "serratus
magnus pars caudalis" of Lagothrix may be
more active in arm-raising than that of Ateles
'Stern et :,I. 1'77)report on a kind of nonpendul'ir arrnhwinging
Invalvingsusta,nedflexionatthuelhowduringhoth.suppiirt;ind swing
phase
33 1
EMG OF SERRATUS ANTERIOR
MIDDLE DIGITATION
I
CAUDAL DIGITATION
I
SUPPORT (15)
SWING (I 8 )
Fig. 7. Phasic activity patterns of middle and caudal digitations of the serratus anterior in a woolly monkey
climbing a vertical trunk [symbols as in Fig. 6). It can be seen that the middle digitation acts in swing phase
presumably to effect the scapular rotation accompanying elevation of the limb to grasp a new hold. The activity of
the caudal digitation is biphasic. A burst occurs in the support phase and is prohably propulsive. A second burst
helps to initiate the swing phase of the cycle.
I
MIDDLE
DIGITATION
L
SUPPORT ( 1 1 )
1 INTERMEDIATE
L
SWING (9)
DIGITATION
SUPPORT (10)
SWING (131
C AU 0A L DIG I TAT I0N
SUPPORT (11)
SWING (9)
Fig. 8. Phasic activity patterns of middle, intermediate, and caudal digitations of the serratus anterior of a
spider monkey during armswinging (symbols as in Fig. 6). The two specimens of Ateles exhibited virtually
identical patterns of muscle activity. As in the vertical climbing, the middle digitation is operative in the swing
phase of the cycle, presumably to effect scapular rotation as the animal reaches for a new grasp. The caudal
digitation acts in the support phase, prohably to pull the trunk up toward the branch. The intermediate digitation
was so desibmated because its activity pattern was found to be intermediate to the other two.
332
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, AND ANDREA K. VANGOR
MIDDLE DIGITATION
-
I
CAUDAL DIGITATION
I
SUPPORT(I1)
SWING(9)
Fig. 9. Phasic activity patterns of the middie and caudal digitations of the serratus anterior in the woolly
monkey during suspended quadrupedalism (symbols as in Fig. 6).The data for the middle digitation are derived
from a different experiment than those for the caudal digitation. The role of the middle digitation in the swing
phase ofthe cycle, and that ofthe caudal digitation in the support (propulsive)phase is illustrated. This distinction
was seen in other previously figured behaviors.
because scapular rotation is more necessary in
the woolly than spider monkey. It now appears
that it was simply a matter of the lower digitation of Lagothrix being slightly more rotatory
due to their less craniocaudal orientation. Had
fibers with a similar orientation been sampled
in the spider monkey, they would have shown
marked activity in elevation of the arm.
The high incidence of only slight activity or
electrical silence observed by Tuttle and Basmajian 1'77) in serratus anterior pars caudalis
of great apes during arm-raising would be expected if they had sampled from caudal digitations. They noted high activity only occasionally, and then a t the onset of movement. This is
confirmed by our data. Surprising in the findings of Tuttle and Basmajian ('77, '78) is the
virtual electrical silence of the serratus anterior pars caudalis in hoisting behaviors and
also quadrupedal locomotion. Their studies discovered no important function for this large
muscle segment having undergone notable
evolutionary change.
Having determined that the lower digitations of serratus anterior are predominantly
active in the propulsive effort of all kinds of
locomotion that were tested, one may comment
on the significance of evolving increasing craniocaudal orientation of these digitations,
either as a consequence of change in thoracic
shape alone (e.g.,Ateles,Pongo) or such change
associated with origin from lower ribs (e.g.,Pan
troglodytes, P a n gorilla).
It is our suggestion that the main benefit of
increasing craniocaudal orientation is to ena-
ble recruitment of the lower digitations as propulsive muscles with diminished tendency to
pull the scapula ventrally. The cineradiographic studies of Jenkins ('74) on quadrupedalism in the rat and of Jenkins et al. ('78) on
brachiation in the spider monkey show a fundamental difference in scapulothoracic movement. In the rat, the support (or propulsive)
phase of locomotion is associated with a uentrocaudal displacement of the scapula on the chest
wall. This displacement coincides with the pull
of obliquely disposed digitations of serratus anterior. On the other hand, in armswinging by
the spider monkey, the scapula shifts dorsocaudally on the trunk. Such a movement is
compatible with the pull of the latissimus dorsi
(transmitted across the shoulder joint), but is
opposite to that of obliquely disposed digitations of serratus anterior and to pectoralis
major. Indeed, in armswinging, latissimus
dorsi is far more active than is pectoralis major
(Stern et al., '77) and is even assisted by the
caudal portion of trapezius (Jungers and Stern,
unpublished data) which attaches directly to
the scapula. If one assumes that additional assistance by the serratus anterior for dorsocaudal scapular retraction is desirable, then it
would be of advantage to the spider monkey to
reduce the counterproductive ventral pull of
this muscle. Such will be the case if the caudal
digitations of serratus anterior become aligned
more parallel to the long axis of the trunk.
It is unfortunate that no data exist for scapulothoracic movement in other suspensory behaviors, such as vertical climbing. It might
333
EMG OF SERRATUS ANTERIOR
I MIDDLE
DIGITATION
SUPPORT (12)
SWING (12)
CAUDAL DIGITATION
SUPPORT (12)
SWING (12)
Fig. 10. Phasic activity patterns of a middle and caudal digitation of serratus anterior in a howling monkey
during quadrupedalism along a horizontal trunk (symbols as in Fig. 6). The middle digitation has a short burst,
just beyond the midpoint of the swing phase, presumably toeffect scapular rotation a s the animal reaches to grasp
a new hold. The caudal digitation exhibits a small burst of activity in the support phase. In Lagothru, and
especially inAtde.5, the support phase activity of the caudal digitation is often accompanied by recruitment of the
middle digitation. The function of serratus anterior pars caudalis during the support phase of quadrupedalism
may be either propulsive or stabilizing.
seem that dorsocaudal displacement of the
scapula would be valuable in vertical climbing
because it would enhance propulsion and concomitantly shift the center of gravity of the
body closer to the support. However, the variation in recruitment of the caudal digitation of
serratus anterior exhibited by our two spider
monkeys during vertical climbing, and the absence of any major role for caudal trapezius
during the support phase of this behavior iJungers and Stern, unpublished data), do not favor
interpretation of the structural evolution of
serratus anterior in terms of a specific response
to the demands of vertical climbing.
A craniocaudal orientation of the lower digitations of serratus anterior is most pronounced
in the great apes. They are not the most expert
brachiators, although their great bulk may
place increased importance on the ability to
recruit an additional muscle (i.e., serratus anterior) to assist in dorsocaudal scapular retraction. These primates also exhibit the highest
degree of thoracic widening (Schultz, ’56),with
attendant location of the scapula on the dorsum
of the chest wall. It may be that the value of
possessing caudal digitations of serratus anterior aligned with the long axis of the trunk is
related to chest shape and scapular positioning.
We might speculate that the more dorsally
placed is the scapula, the less tolerable are ventral and lateral components to its caudal re-
traction. Further studies on the great apes are
required to test this possibility. At the moment,
all we can assert with confidence is that progressive craniocaudal orientation of the lower
digitations of serratus anterior is related to
propulsion and not to arm-raising.
The serratus anterior of humans is similar in
relative bulk to this muscle in “brachiators”
(Ashton and Oxnard, ’63). On the other hand,
despite a broad thorax and dorsally placed
scapulae in humans, the orientation of the
lower digitations of serratus anterior is n o more
craniocaudal than in a variety of monkeys. In
its current state, the human serratus anterior
pars caudalis seems clearly adapted for armraising functions. It lacks the specializations
associated with suspensory behavior in largebodied, broad chested nonhuman primates. If
such specializations have not been lost, we can
interpret the modern human condition a s
suggesting descent from a small ape with a
thoracic shape similar to atelines. The remarkably broad thorax of humans would then be a
trait evolved in conjunction with bipedality and
convergent on the condition of the great apes.
AC K NO W I,E DGMENTS
We extend our appreciation to Ms. Lorraine
Rice for her valuable technical assistance and
to Ms. Lucille Betti and Leslie Jungers for producing the illustrations. We are also indebted
334
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, AND ANDREA K. VANGOR
to the Los Angeles Zoo for permitting us to use
one of their specimens ofAlouatta seniculus in
our experiments. This study was supported by
NSF Research grant BNS 7683114A01.
LITERATURE CITED
Ashton, E.H., and C.E Oxnard (1963) The musculature of
the primate shoulder. Trans. 2001. SOC.
(London)29:55%
650.
Ashton, E.H., and C.E. Oxnard (1964) Functional adaptations in the primate shoulder girdle. Proc. Zool. Soc. (London) 142:4%66.
Ashton, E.H., M.J.R. Healy, C.E. Oxnard, and T.F. Spence
(19651 The combination of locomotor features of the primate shoulder girdle by canonical analysis. J. Zool.,
147:40&4'29.
Jenkins, F.A., J r . il9741 The movement of the shoulder in
claviculate and aclaviculate mammals. J. Morphol.,
144:7 1-84.
Jenkins, F.A. J r . , P.J. Dombrowski, and E.P. Gordon (1978)
Analysis of the shoulder in brachiating spider monkeys.
Am. J. Phys. Anthrop., 48:65-76.
Kohlbnigge, I.H.F. i 1890) Muskeln und periphere Nerven
des G n u s Hylohnfes. E.J. Brill, Leiden.
Kohlbriigge, I.H.F. i 1897) Muskeln und periphere Nerven
der Primaten, mit besonderer Berucksichtigung ihrer
Anomalien. Verh. Akad. Wet. Amsterdam, Sect. 2, vol. 5 ,
no. 6, 264 pp.
.
J.
Miller, K.A. i 19521 The musculature ofPnn p o n ~ s c u s Am.
Anat., 91.18:%2:32.
Oxnard, C.E. (1967) The functional morphology of the primate shoulder as revealed by comparative anatomical,
osteometric, and discriminant function techniques. Am. J.
Phys. Anthropol., 26:21%240.
Primrose, A. (1898-18991The anatomy of the Orang outang
(Suninsatyrus), a n account of some of its external characteristics, and the myology of the extremities. Trans.
Canad. Inst. (Toronto), 6:507-598.
Raven, H.C. I 19501 The anatomy of the gorilla. Columbia
Univ. Press, New York.
Schultz, A.H. (19561 Postembryonic age changes. In H.
Hofer, A.H. Schultz, and D. Starck, teds.): Primatologia. I.
Systematik, Phylogenie, Ontogenie. Karger, Basel, pp.
887-964.
Stern, J.T. Jr., J.P. Wells, A.K. Vangor, and J.G. Fleagle
i 1977) Electromyography of some muscles of the upper
limh in Ateles and Lnglothrix. Yrhk. Phys. Anthropol.,
20:49%507.
Stern, J.T. Jr., J . P . Wells, W.L. Jungers, A.K. Vangor, and
J.G. Fleagle (1980) An electromyographic study of the
pectoralis major in atelines and Hylohotr. with special
reference to the evolution of ii pars clavicularis. Am. J .
Phys. Anthropol. ,52.1%25.
Stewart, T.D. (19361 The musculature of the anthropoids. I.
Neck and trunk. Am. J. Phys. Anthropol. 21:141-204.
Tuttle, R.H., and J . V . tlasmajian (19771Electromyography
of poned shoulder muscles and hominoid evolution. I. Retractors of the humerus and rotators of the scapula. Yrbk.
Phys. Anthropol., 20: 49 1-49 7.
Tuttle, R.H., and J.V. Basrnajian I 19781 Electromyography
of pangid shoulder muscles. 111. Quadrupedal positional
behavior. Am. J. Phys. Anthropol., 49.57-70.
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