close

Вход

Забыли?

вход по аккаунту

?

An electromyographic study of the pectoralis major in Atelines and Hylobates with special reference to the Evolution of a pars clavicularis.

код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 52:13-25 (1980)
An Electromyographic Study of the Pectoralis Major in
Atelines and Hylobates, With Special Reference to the
Evolution of a Pars Clavicularis
JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS,
ANDREA K. VANGOR, AND JOHN G. FLEAGLE
Department of Anatomical Sciences, Health Sciences Center, State University of
New York a t Stony Brook, Long Island, N e w York 1 1 794
KEY WORDS Electromyography, Pectoralis major,
Atelines, Hylobates, Evolution
ABSTRACT
Among primates there is striking variation in the extent of the
origin of pectoralis major from the clavicle. A significant clavicular attachment
(pars clavicularis) occurs only inillouattu, Lugothrix, Hylobates, Pan (troglodytes,
paniscus andgorilla), and Homo. Interpreting this trait in nonhuman primates as
an adaptation to frequent use of a mobile forelimb in climbing and suspension is
contraindicated by the absence of a clavicular origin in Ateles andPongo. We have
undertaken a telemetered electromyographic study to determine any special role of
the most cranial part of the pectoralis major in comparison to its caudal part, and to
the deltoid, during vertical climbing, pronograde quadrupedalism, and armswinging in Ateles, Lagothrix, Alouatta, andHylobates. The results show that the cranial
pectoralis major possesses a role not shared by the caudal fibers: initiation of the
recovery phase of the locomotor cycle. When ability to execute rapid or powerful
recovery of the adducted forelimb is required in an animal with a shoulder joint
lying on a plane cranial to that of the manubrium, the movement will be facilitated
if the origin of the pectoralis major is extended onto the clavicle. Such is the case in
nonhuman primates possessing this trait. The absence of a clavicular origin in
Ateles and Pongo may be related to diminished selective pressures to perfect
locomotor modes such as pronograde quadrupedalism, armswinging, or climbing
thick vertical trunks, that demand rapid or powerful recovery of the adducted
forelimb. If the arboreal ancestor of humans had evolved a clavicular origin of
pectoralis major, this animal would be preadapted for certain uses ofthe forelimb in
its bipedal descendant.
The anthropoid apes and prehensile-tailed
New World monkeys are remarkable among
primates for the high degree to which they
practice behaviors such as climbing, hanging,
and swinging that impose mechanical demands
for a mobile forelimb able to resist tensile forces
(reviewed in Stern and Oxnard, '73). The same
animals share a number of anatomical traits
that seem to be adaptations for these special
locomotor abilities ( Washburn, '63; Erikson,
'63; Oxnard, '67; Stern, '71). In 1963 Ashton and
Oxnard published their now classic monograph
in which the shoulder musculature of primates
was examined in order to identify such adaptations. Among the muscles that were characterized by functionally interpretable morphological variation was the pectoralis major.
Ashton and Oxnard emphasized differences in
fiber direction, caudal extent of origin, and relative thickness of the cranial versus the caudal
portions of pectoralis major. These were interpreted as reflecting a dichotomy between use of
the forelimb in a low, relatively retracted posi0002-9483/80/5201-0013 $02.60 0 1980 ALAN R. LISS, INC.
tion as is most common in generalized running,
jumping, pronograde primates, and use of the
forelimb in a raised abducted position, as in the
climbing-hanging apes and prehensile-tailed
cebids.
One striking variation that Ashton and Oxnard did not interpret was the extent of the
origin of pectoralis major from the clavicle. A
noteworthy clavicular origin (pars clavicularis,
Fig. 1) occurs solely in anthropoid primatesl,
and within this group only among a few genera.
Table 1 lists primates according to whether or
not they possess a significant clavicular origin
of pectoralis major. Interpretation of the distribution is difficult because the anatomical
groups seem not to have any clear relation to
James P Wells is presently at West Virginia School of Osteopathic
Medicine, Lewisburg, West Virginia 24901
'Jouffroy ('62) reports an attachment o f t h e pectoralis major to the
proximal third of the clavicle In Malagasy prosimians, but Ashton and
Oxnard ('63i, and our observations on Lemur cutta, L. fuluus. and
Propithecus irerreuuxi .ndicate no fibers arising more laterally than the
extreme medial end of this bone.
13
JACK T. STERN, JR., ET AL.
14
WOOLLY
MONKEY
SPIDER
MONKEY
Fig. 1. The pectoralis major in the spider monkey iAtelesi and woolly monkey tlagothrinl. Note the absence of
any attachment to the clavicle in the spider monkey and the presence of an origin from the medial half of the
clavicle in the woolly monkey. The only other primates with a significant clavicular origin of pectoralis major are
Alouatta, Hylobates, Pan troglodytes, P . paniscus, P . gorilla. and Homo.
TABLE 1. Distribution of Clavicular
Origin of Pectoralis Major
Among Primates
Significant clavicular
origin present
Howling monkey
Woolly monkey
Gibbon
Siamang
Chimpanzee
Gorilla
Human
No significant
clavicular origin
Prosimians
Old World monkeys
Non-prehensile-tailed
New World monkeys
Spider Monkey
Orangutan
locomotor behavior. In particular, the absence
of a clavicular origin in spider monkeys and
orangutans deters one from explaining its
presence as a n adaptation to frequent use of the
forelimb in arboreal climbing and suspension.
The failure of the classical comparative
method to discover the significance of a clavicular origin of pectoralis major has prompted us
to apply experimental techniques toward a solution of this problem. We have undertaken a n
electromyographic study to discover any special role of the cranial part of the muscle in
relation to its caudal part. To date, the only
electromyographic investigation of the pectoralis major in nonhuman primates has been
that of Tuttle and Basmajian ('77, '78) on the
three great apes. These authors confined their
examination to the sternocostal (caudal) por-
tion of the muscle, observing that it is active in
hoisting, is also a regular supporter of the
upper body weight, and is probably also a propulsive element during quadrupedal walking.
In this paper we present results of a study of
both the cranial and caudal pectoralis major,
along with the acromiodeltoid, in the spider
monkey (Ateles), woolly monkey (Lagothrix),
howling monkey (Alouatta), and gibbon (Hylohates).
MATERIALS AND METHODS
Subjects
The subjects for t h e electromyographic
experiments were three spider monkeys ( 1 d A .
fusciceps, 2 ? A . belzebuth), two woolly monkeys (1d a n d 19 L. lagothricha), one howling
monkey ( ? A . seniculus), and two gibbons
( l d a n d 19 H.lar.). All subjects were adult (the
howling monkey rather aged) showing no obvious pathology. The New World monkeys had
been housed in a large enclosure (7.3m x 3.7m
x 2.7m) for at least six months prior to study.
The gibbons lived in this came cage for approximately one month before study. Within the
enclosure were a long horizontal tree trunk
(7.3m x 9.5cm), placed approximately 60cm
above the ground, a long vertical tree trunk
(3.7m x 8.5cm), and a 7.3m long ladder with
wooden dowel (2.8cm diameter) cross pieces
spaced 40cm apart suspended from the roof of
EMG OF PECTORALIS MAJOR
the cage. The subjects had become well accustomed to locomotion on these supports by
the time of the experiment. They were induced
by means of food reward to locomote on specific
substrates. Spider monkeys and gibbons
readily engaged in armswinging beneath the
ladder. Of the woolly monkeys, only the male
would perform “pendular” armswinging; this
behavior was infrequent and the wire mesh of
the cage roof was the substrate. Climbing the
vertical trunk was performed by the spider
monkeys, woolly monkeys, and gibbons. In
addition, these animals would spontaneously
ascend the wire mesh sides of the cage, as would
t h e howling monkey. Pronograde quadrupedalism along the horizontal branch was
practiced by all three monkeys, but not by the
gibbons.
METHODS
We employed the technique of telemetered
electromyography described by Stern et al.
(’77). This technique permits the subjects to
locomote freely and naturally without the hindrance of wires running from the animal to a
recording device. Two important modifications
were incorporated into this study. One concerns
the method by which proper placement of electrodes was verified, the other pertains to analysis of data.
Electrode Placement
In the experiments on spider and woolly
monkeys, we relied on the ease with which the
muscles could be palpated to satisfy the demand for accurate placement of fine wire electrodes. Although the pectoralis major and
acromiodeltoid are also easily palpated in howling monkeys and gibbons, we introduced an
additional means of verification by passing a
small stimulating current through the fine
wires following their insertion into the muscle
belly (i.e.,back-stimulation). Clear contraction
of the relevant muscle portion was elicited and
served to confirm position of the electrode.
The data presented below were derived from
electrodes placed in the following three locations: a) as close as possible to the cranial edge
of the pectoralis major half way between its
origin and insertion; b) into the caudal edge of
the pectoralis major in the anterior axillary
fold; c) into the deltoid muscle half way along a
line between t h e acromion process of t h e
scapula and deltoid tuberosity of the humerus.
Records were also obtained from the portion of
the deltoid arising from the lateral end of the
clavicle but are omitted here because they do
15
not add to the resolution of the questions posed
in this paper.
Data Analysis
Because we were able to study more than one
representative of three of the four genera, and
often obtained data for a sizeable number of
“step”cycles of each of the locomotor modes, we
obtained considerable information about variability ofmuscle recruitment. In order to assess
this variability in a more objective manner, the
data analysis was modified from that described
in Stern et al. (’77).This first involved a technical change in the videotape recording process
such that a t the end of every sweep of the oscilloscope beam the superimposed picture of the
subject was deleted and an unobscured image of
the previous two seconds of EMG was displayed
on the video monitor. A paper copy of this image
was reproduced by a Tektronix 4632 video hard
copy device. On the paper copy were marked
exactly the times when limbs contacted the
substrate and when they were in midsupport
and midswing. These data were then analyzed
by tracing the actual shape of the electromyographic interference pattern with the stylus of
NT-501 Sonic Digitizer (Science Accessories
Corporation, Southport, Connecticut) and entering this information, along with that for
locomotor events, into a Hewlett-Packard 9830
computer. The computer constructed a 20 x 20
matrix with the columns representing equal
intervals within a phase of support (when the
tested limb is in contact with the substrate), or
swing (when the tested limb is free of the substrate and moving forward to grasp a new hold),
and the rows representing equal intervals of
level of activity (the maximum being the largest burst of EMG observed during the entire
experiment). If n samples of activity during a
given phase of a given behavior are available
and traced with the digitizer stylus, the computer fills in a square of the 20 x 20 matrix in
every instance when activity occurs in that
square. After all n samples have been digitized,
the computer calculates the per cent incidence
of activity of a given level at a given point in the
phase. The result is an output indicating the
variability in electromyographic activity. The
data for different subjects of the same genus are
used to derive a composite picture of variability
for that genus. Text figures are reproduced
from these composites. Blackened regions indicate highly consistent presence of EMG activity, occurring ?hor more of the time on the
average. Enclosed white regions indicate frequent but not consistent activity, occurring a t
least half of the time in one subject.
JACK T. STERN, JR., ET AL.
16
This method of quantification allows accurate assessment of variability in onset and
cessation of EMG activity but is somewhat
novel in its approach to judging amplitude.
What is digitized by our methods is the visual
appearance of the EMG burst. The taller this
burst appears, the greater will be judged the
amplitude of EMG. Such a relationship is to be
expected, since larger and more frequent spikes
will summate to taller bursts. Nonetheless, in
one instance we performed an experiment in
which the EMG signal was passed through a
full-wave rectifier and averager. Figure 2
presents five EMG bursts of increasing
amplitude along with their rectified averaged
signals and the shape of these bursts as we
would trace them for digitization. It can be seen
that the method of tracing yields a picture of
relative amplitudes that in general parallels
that presented by the averaged signal. We believe our method is as accur.ate as grading activity into categories of relative amplitude
(e.g.,nil, negligible, slight, moderate, marked)
and is less subjective.
RESULTS
Climbing a Vertical Trunk
This mode of locomotion generally elicits the
highest levels of phasic activity, and the recruitment patterns during climbing illustrate
very clearly the separate roles of the cranial
and caudal parts of the pectoralis major (Fig. 3).
In Ateles, Lagothrix, and Hylobates the caudal
portion of the pectoralis major is propulsive in
its action throughout most of the support phase,
or pull-up. It is worth noting (although not illustrated here) that the level of activity in
caudal pectoralis major is substantially less
during the support phase of climbing when this
activity is performed on the wire-mesh side of
the cage rather than on the vertical trunk. Such
a difference may be related to the fact that
there is reduced adduction at the shoulder during the pull-up of cage climbing because the
animal is not constrained to grasp the substrate
directly ventral to its thorax.
The cranial portion of the pectoralis major
shares with the caudal portion the ability t o
adduct and retract the forelimb from the raised
position, but, as can be noted for all genera in
Fig. 3, the activity in the cranial portion ceases
earlier in the support phase due to the fact that
its retractive abilities disappear at a relatively
more elevated position of the forelimb. Figure 3
also illustrates the fact that the propulsive activity of the cranial pectoralis major persists
somewhat longer in Ateles, presumably due to
the fact that in this animal the sampled fibers
arise from the manubrium and not the clavicle,
and therefore have an orientation that permits
them to exert a retracting moment with the
arm in a lower position.
In all three genera, the unique role of the
cranial pectoralis major is to initiate the recoueryphase of the limb as it reaches to grab a new
hold higher on the vertical trunk. In the woolly
monkey the fibers arising from the clavicle are
predominantly active during the recovery, or
swing, phase and are almost solely responsible
for this movement. By contrast, in the spider
monkey, the deltoid plays a major role in recovery later in the movement. This distinction is
probably related to the different manners in
which these animals climb (Fig. 4). The spider
monkey tends to hold its arm abducted at the
shoulder during the recovery phase of the cycle,
whereas the woolly monkey climbs with the
forelimb in a relatively adducted position. The
basis for this difference might lie in the more
lateral orientation of the glenoid in the spider
monkey, its greater interglenoid distance relative to diameter of the support, and its longer
arms. As a consequence, the spider monkey relies more on the deltoid, an abductor, to effect
recovery than does the woolly monkey. The distinction is even clearer when these animals
climb the wire mesh side of the cage, a behavior
demanding less constant adduction. In this circumstance the activity of the cranial pectoralis
during recovery is reduced in both Ateles and
Lagothrix, but far more so in the former.
In the gibbon, as in the spider monkey, recovery phase during climbing involves abduction
at the shoulder, and this is reflected by the
consistent activity of the deltoid during this
phase. However, the cranial pectoralis of the
gibbon plays a greater role in recovery than
does that of the spider monkey. The explanation for this may be: 1)that the fibers arise from
the clavicle and therefore have an orientation
permitting them to continue protraction up t o a
more elevated position of the arm; and 2) that
the relatively long and heavy forelimb of the
gibbon requires the force of both pectoralis
major and deltoid to effect recovery.
Pronograde Quadrupedalisrn Along a Branch
That the cranial portion of the pectoralis
major has as its unique role flexion of the
adducted upper limb is supported by the records
of muscle activity during pronograde quad-
TRACED
EMG
EMG
RECTIFIED
AVERAGEDEMG
Fig. 2. A comparison of two methods of “quantifying” the amplitude of EMG activity. The top curves represent electronically rectified and averaged transformations of EMG burstsjust below. The bottom curves represent the results of tracing
the outlines of the bursts as we have done in this paper. I t can be seen that our method of tracing yields a picture of relative
amplitudes that in general parallels that presented by the electronically averaged signal.
c
-3
Deltoid
Cranial
Pectoralis
Major
Major
PeLtoralis
Caudal
I
I
SWING
(3-52)
SWING
UPPORT
(2-25)
I(2-27)
SUPPORT
I
R
SUPPORT
h
I
W 00 LLY MONKEY
I
I
SWING
(2-251
(2-33)
SWING
(2 - 26)
SWING
!-
,
GIBBON
A
,UPPORT
(2-6)
SUPPORT
(2-7)
Fig. 3. Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Ateles, Lagothrzx, and
Hylobates during climbing a vertical tree trunk. Blackened areas indicate highly consistent presence of EMG activity; enclosed white
areas indicate frequent but less consistent activity. The heights of these areas reflect amplitude of activity; the maximum amplitude
observed during the experiment is represented by the height of the vertical line at the beginning of SUPPORT. Two numbers appear
under the words "SUPPORT' and "SWING". The first is the number of animals from which data were derived for this phase, the second is
the number of phases (support or swing, respectively) digitized to yield the composite picture of activity.
Note that although the cranial pectoralis major assists the caudal portion of the muscle in pulling the animal up during climbing, the
unique role of the cranial fibers are in the swing (recovery) phase of locomotion.
r _ _ l
SPIDER MONKEY
I
I
L
A
(3-50)
SUPPORT
CLIMBING VERTICAL TRUNK
SWIN(
SWING
(2-10) I
c
a,
EMG OF PECTORALIS MAJOR
rupedalism in Ateles, Lagothrix, and Alouatta
(Fig. 5). As in climbing the vertical trunk, the
function of the caudal portion of pectoralis
major is propulsive. Furthermore, in our two
woolly monkeys, which move rather quickly,
the caudal pectoralis major begins its contraction substantially before touch-down in order to
decelerate t h e swinging limb. I n quadrupedalism along a branch, the special role of
the cranial pectoralis is in the recovery phase of
the cycle. Figure 5 shows how this role is accentuated in woolly monkeys in which the forelimb
is more adducted during swing than in the
spider moneky (Fig. 6). The deltoid, an abductor, is more consistently active during the recovery of the limb in Ateles than in Lagothrix.
The burst of deltoid activity in the second half
of the swing phase in Alouatta is not accompanied by abduction of the arm at this point in
locomotion. Rather, the acromiodeltoid of howling monkeys acts in swing phase probably as a
simple protractor of the limb. This is due to the
orientation of the scapula more along the side of
a dorso-ventrally deep chest in howling monkeys. It shares this orientation, but in a less
extreme manner, with more typically quad-
W O O L L Y MONKEY
19
rupedal primates such as Old World monkeys
and non-prehensile tailed cebids.
Armswinging
Although neither portion of the pectoralis
major is active during quiet suspension by the
forelimbs, armswinging is characterized by
consistent recruitment of this muscle. Figure 7
presents the records of muscle activity during
non-richochetal armswinging for Ateles,
Lagothrix, and Hylobates2. The data support
the conclusion drawn from the other locomotor
modes.
The caudal pectoralis is active a t a low level
during the support phase ofmovement (our two
gibbons differed dramatically in amplitude of
activity). Interestingly, in gibbons there also
occurs a small burst at the onset of recovery
when the hand is just released from the substrate. This burst probably provides a brief impulse of acceleration to enable a rapid recovery
phase.
AOurgibbons also engaged in richochetal armswinging. The diNerences In muscle recruitment between this behavior and dower armswinging will be the subject of a separate paper.
SPIDER MONKEY
Fig. 4. Drawings of the limb positions inLag0thri.x and Ateles during climbing a narrow vertical trunk. Note
that in the swing (recovery)phase of locomotion, the forelimb is held adducted in the woolly monkey but abducted
in the spider monkey.
Middle
Deltoid
Cranial
Pec tora I i s
Major
Caudal
Pectoralis
Major
I
SWING
( 3- 67)
SWING
(2-83)
/-
I
UPPORT
(2-38)
UPPORT
(2-55)
(2-40)
I
I
1
(1-65)
SUPPORT
(1-27)
I
I
HOWLING MONKEY
(1-64)
I
I
(1-39)
SWING
2
1
/
4
1
WOOLLY MONKEY
Fig. 5. Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Ateles, Lugothrix, and
Alouattn during pronograde quadrupedalism along a horizontal tree trunk (see legend to Fig. 3 for explanation of symbols). This figure
has been constructed so t h a t midsupport corresponds to placement of the shoulder directly above the wrist and midswing to placement of
the wrist directly beneath the shoulder.
Note that the special role of the cranial pectoralis major is in the swing (recovery)phase of the locomotor cycle, as was also the case for
vertical climbing.
(2-79)
SUPPORT
1
SUPPORT
(2-48)
PRONOGRADE QUADRUPEDALISM ALONG HORIZONTAL TRUNK
E3
r
R
.e
C
EMG OF PECTORALIS MAJOR
WOOLLY MONKEY
21
SPIDER M O N K E Y
Fig. 6. Drawings of the limb position in Lugothrix and Ateles during pronograde quadrupedalism along a
horizontal tree trunk. Note that in the swing (recovery) phase of the locomotor cycle, the forelimb is held adducted
in the woolly monkey but partially abducted in the spider monkey.
During armswinging the cranial pectoralis
major appears to serve different roles in the
three different genera. In the spider monkey,
this muscle segment frequently (but not consistently) contracts in the vicinity of midswing to
promote elevation of the limb. However, the
major work of forelimb elevation occurs later in
the recovery and is effected by the deltoid. The
data for Lagothrix are sparse, but suggest a
rather complicated recovery stroke involving a
reciprocal interaction between deltoid and cranial pectoralis major.
Hylobates, the primate arm-swinger par excellence, differs from the New World genera in
possessing consistent support phase activity of
cranial pectoralis major. The burst at the onset
of this phase occurs in both gibbons and spider
monkeys, but more consistently in the former.
This may be attributed to shock-absorption at
touch-down, although it is possible to interpret
this as evidence for a regulated abduction of the
shoulder under the influence of gravity. More
interesting is the regular burst of cranial pectoralis activity i n the gibbon just after midsupport. An accentuation of caudal pectoralis activity is also seen a t this time and both are
related to a pull-up (Fig. 8) which occurs in the
gibbon at this point during amswinging. Such
a pull-up serves to elevate the center of gravity
to enable the animal to rise higher a t the end of
the support phase for the purpose of permitting
a greater drop, and thus greater acceleration
due to gravity, during the next following cycle
(Fleagle, '77).
The greatest amplitude of cranial pectoralis
major activity during armswinging in the gibbon occurs a t midswing. Tnis burst is essential
to effect a rapid recovery of the long forelimb,
which is adducted a t the shoulder and flexed a t
the elbow to diminish moment of inertia. It can
be seen from Figure 8 that the recovery phase of
the spider monkey does not involve the attempt
to reduce moment of inertia that characterizes
gibbons. This, along with the absence of the
initial impulse provided by the caudal pectoralis major, implies a more loosely programmed recovery phase in the spider monkey.
The two genera do resemble one another in the
role of deltoid to produce the terminal movement of recovery.
DISCUSSION
Electromyographic records of the pectoralis
major in Ateles, Lagothrix, Alouatta, and Hylo-
Major
PPctoralii
Caudal
I
I
SUPPORT
(1-5)
I
WOOLLY MONKEY
(1-12)
SWlNC
(1-9)
SWING
(2-11)
SUPPORT
SUPPORT
(2-32)
(2-17)
SUPPORT
I
GIBBON
Fig. 7 . Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Aleles, Lugothrzx, and
Hylobutes (see legend to Fig. 3 for explanation of symbols). This figure has been constructed so that midsupport corresponds to placement
of the shoulder directly beneath the point of support and midswing corresponds to placement of the elbow directly beneath the shoulder
(see Fig. 8).
Note that in the gibbon, the cranial pectoralis major has a special role in the swing (recovery)phase ofthe locomotor cycle. Additionally
it joins with several other muscles (not illustrated here) in effecting a pull-up just after midsupport. The late support and midswing
phases of activity of cranial pectoralis major are only inconsistently present in spider monkeys.
SWING
(3-491
mel)
SWING
SUPPORT
(1-11)
k
iUPPORT
(3-44)
SUPPORT
SPIDER MONKEY
ARM SWINGING
SWING
(2-45)
1
SWING
(2-23)
23
EMG OF PECTORALIS MAJOR
SPIDER MONKEY
2
1
3
5
4
GIBBON
1
2
c
3
4
5
_
Fig. 8. Drawings of limb positions during armswinging inAteles and Hylobates. 1 = onset of right limb support phase, 2 =
midsupport by right forelimb, 3 = end of right limb support phase, 4 = midswing of right forelimb, 5 = onset of right limb
support phase.
Though several differences are illustrated, ofgreatest significance for the present study are: 1) the pull-up executed by the
gibbon in the second half of the support phase; and 2) the adducted arm and flexed forearm of the gibbon during swing phase.
Both behaviors represent part of a "perfected'mechanism for armswinging. The first serves to elevate the center ofgravity to
enable the animal to rise higher a t the end of support phase for the purpose of permitting a greater drop, and thus greater
acceleration due to gravity, during the following cycle (Fleagle, '77). The position of the forelimb during swing phase reduces
its moment of inertia and enables a rapid execution of recovery.
bates during vertical climbing, pronograde
quadrupedalism, and armswinging demonstrate that although the cranial portion of the
muscle assists the caudal portion during retraction of the previously protracted (elevated)
forelimb, the unique role of the cranial portion
is for flexion of the adducted forelimb as required in the recovery phase of the locomotor
cycle. Does knowledge of this unique role help
us to explain why in some primates the origin of
the pectoralis major has extended far onto the
clavicle,whereas in others an attachment to the
manubrium suffices?
A clavicular origin of pectoralis major might
be necessary to promote flexion of the forelimb
in animals in which the humeral insertion of
the muscle is on the same transverse plane as,
or cranial to, the manubrium. Such will be the
case during much of the locomotor cycle in primates that have a shoulder joint cranial to
t h e level of t h e manubrium. Schultz
('26, '33, '56) provides values of a
" l
L4
JACK T.STERN, JR., ET AL
ratio called relative shoulder height,
which is calculated by dividing the distance
between the suprasternal notch and interacromial line by the anterior t r u n k
height, then multiplying by 100. The larger the
value of this index, the more cranial is the
shoulder joint relative to the manubrium.
Schultz notes that high values characterize the
apes (Hylobates = 13, Pongo = 16, Pan troglodytes = 17, P. gorilla = 13), spider monkeys
(Ateles = lo), and howling monkeys (Alouatta
= 131, whereas a low value (51, indicating a
shoulderjoint near the same level as the manubrium, characterizes Old World monkeys and
Saimiri. Figure 3 of the monograph by Schultz
('56) indicates a similarity between Old World
monkeys and prosimians. Our measurements
on one spider monkey, two woolly monkeys,
and one howler, all under anesthesia, yield
values for the shoulder height index of 16, 13,
and 11 respectively for these genera. An
additional line of evidence is provided by Jenkins, et al. ('78) who demonstrated radiographically that the level of the shoulder joint
lies far cranial to the sternoclavicular joint in
Ateles during hanging by the forelimb, whereas
in Macaca, Cercopithecus, and Saimiri even
this behavior is insufficient to displace the joint
cranially.
The distribution of a cranially displaced
shoulderjoint suggests very strongly that it is a
trait associated with remodelling of the shoulder complex for the enhanced mobility required
by primates that employ their upper limb in
climbing and suspension.:'
Among nonhuman primates, it is only those
with cranially displaced shoulder joints that
possess a significant clavicular origin of pectoralis major. Nonetheless, within this group,
the spider monkey and orangutan have not
evolved this trait. The explanation for the absence of a clavicular origin of pectoralis major
inAteles and Pongo may be that the behavior of
these animals does not demand particular facility for flexion of the adducted forelimb. Such
facility is required for rapid pronograde progression either in the trees (Alouatta, Lagothrix) or on the ground (P. troglodytes, P. paniscus, P. gorilla). It is probably necessary for the
ascent of thick tree trunks, a behavior especially important for chimpanzees (Kortlandt,
'75) and bonobos (R. Susman, personal communication). In this regard it is interesting to
note that such behavior is less significant for
gorillas, and that gorillas possess a less extensive clavicular origin of pectoralis major than
"However, Schultz 1'26) attributes the obliquity of the clavicles
among howling monkeys to the presence of a greatly enlarged hyold
apparatus.
do chimpanzees (Ashton and Oxnard, '63). Finally, flexion of the adducted forelimb appears
to be a vital element of perfected armswinging
as demonstrated by Hylobates.
Field studies of the spider monkey (Mittermeier and Fleagle, '76; Mittermeier, '78) and
orangutan (MacKinnon, '74) indicate that
these species practice pronograde quadrupedalism less frequently and either less
speedily or more awkwardly than most primates. The same studies give no indication that
ascent of thick vertical trunks is an habitual
positional behavior of selective importance, as
has been argued for chimpanzees and bonobos.
Furthermore, armswinging in the orangutan is
uncommon and the forelimb does not swing beneath the shoulder during recovery. The very
presence of a prehensile tail in Ateles may be
the single most important factor reducing the
demand for mechanical perfection of armswinging. If this animal fails to reach the next
support in adequate time, its safety is insured
by the grasp of the tail.
These considerations lead us to conclude that
evolution of a cranial origin of the pectoralis
major in nonhuman primates is a response to
demands for strength or rapidity of flexion of
the adducted forelimb in animals having
undergone morphologic reconstruction of the
shoulder to enhance upper limb mobility. Although the new muscular attachment has
evolved in nonhuman primates only among
those genera that practice behaviors emphasizing a mobile forelimb able to resist tensile
forces, the need for this attachment is not related to use of the forelimb under tension in the
abducted elevated position. Instead, a clavicular origin of pectoralis major may be viewed as
compensating for the remodeling of the shoulder associated with these behaviors. It is a
strength of the experimental method that it can
elucidate such complex evolutionary mechanisms.
A final consideration is whether or not
studies of the cranial pectoralis major in
nonhuman primates can shed light on the
evolution of Homo, one of those rare primates
with an extensive clavicular origin. Modern
adult Caucasians have a relative shoulder
height index less than 1 (Schultz, '26),i.e., their
shoulder joint is on the same level as the manubrium. However, there is an ontogenetic descent of the shoulder to achieve this state.
Schultz concluded that the fetal condition
suggests the existence of a high shoulder in the
human ancestor. One could speculate that a
clavicular origin of pectoralis major was another characteristic of this ancestor.
Even if the clavicular origin of pectoralis
25
EMG OF PECTORALIS MAJOR
major in humans is a retention of a t r a i t
evolved i n a n arboreal setting, t h e d a t a
presented here do not point to one particular
behavior that must have been practiced in our
past. A clavicular origin of pectoralis major
seems to serve as the “ideal morphology” for
more than one behavior. It may have evolved to
meet the demands of brachiation in gibbons
and pronograde quadrupedalism in certain
prehensile-tailed cebids and African apes. Further impetus to evolution of this trait in chimpanzees and bonobos can be attributed to the
importance for these animals of climbing thick
vertical trunks. The presence of a clavicular
origin of pectoralis major in the arboreal ancestor of humans would imply a shoulder remodeled for mobility, as has been suggested on
numerous other grounds (Washburn, ‘63; Oxnard, ’69), and would detract from any suggestion that portrays this ancestor as being as
completely devoted to quadrumanous climbing
a s the modern orangutan.
Having a relatively low shoulder joint, m d ern humans might not be expected to need a
clavicular pectoralis major. This muscle is still
a flexor of the adducted forelimb (see Basmajian, ’781, but it might be thought that a manubrial attachment would suffice. The distinct
advantage of a clavicular origin in humans
probably is not related to the early stages of
forelimb flexion, as in nonhuman primates, but
to one or both of the following requirements:
1) the ability to resist extension of the markedly flexed arm; 2) the ability to powerfully
adduct the arm without simultaneous extension. The first of these behaviors is an essential
element of forelimb use in carrying large objects. The second is a component of the movement involved in throwing. Permitting ourselves to engage in extreme speculation, we
conclude that the existence of a clavicular origin of pectoralis major in a human ancestor
might be a preadaptation to the ways in which
the forelimb would be used in a bipedal descendant.
ACKNOWLEDGMENTS
Invaluable technical assistance was rendered by Marcy Koltun, William Korosh, and
Lorraine Rice. The illustrations were lovingly
prepared by Lucille Betti. Our special thanks
go to Dr. Robert Gossette, Hofstra University,
who so generously permitted us to conduct experiments on his two gibbons, and to the Los
Angeles Zoo for providing a specimen of the red
howler. This study was supported by NSF Research grant BNS 76831141201.
LITERATURE CITED
Ashton, E.H., and C.E. Oxnard (1963) The musculature of
the primate shoulder. Trans. Zool. SOC.(Lond.), 29:55%
650.
Basmajian, J.V. (1978) Muscles Alive, Their Functions Revealed by Electromyography. Williams and Wilkins, Baltimore.
Erikson, G.E. (1963) Brachiation in New World Monkeys
Lond., No. 10, pp.
and in Anthropoid Apes. Symp. Zool. SOC.
135-163.
Fleagle, J.G. (1977) Brachiation and biomechanics: the
siamang a s example. Malay Nature J., 30:45-51.
Jenkins, F.A., Jr., P.J. Dombrowski, and E.P. Gordon (1978)
Analysis of the shoulder in brachiating spider monkeys.
Am. J. Phys. Anthropol., 48:6676.
Jouffroy, F.K. i1962) La musculature des membres chez les
Lemuriens de Madagascar. Etude descriptive et comparative. Mamrnalia, 26:suppl. 2, pp. 1-326.
Kortlandt, A. (1975)Ecology and paleoecology of ape locomotion. In: Roc . Symp. 5th Int’l. Primat. SOC.
(1974). Japan
Sci. Press, Tokyo, pp. 361-364.
MacKinnon, J. (1974) The behaviour and ecology of wild
orangutans (Pongo pygmaeusi. Anim. Behav., 22:%74.
Mittermeier, R.A., and J.G. Fleagle (1976) The locomotor
and postural repertoires of Ateles geoffroyi and Colobus
guereza, and reevaluation of the locomotor category
semibrachiation. Am. J. Phys. Anthropol., 45:235-256.
Mittermeier, R.A. (1978) Locomotion and posture in Ateles
geofroyr and Ateles paniscus. Folia primat. 30: 161-193.
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., 26:219-240.
Oxnard, C.E. (1969) Evolution of the human shoulder: some
possible pathways. Am. J. Phys. Anthropol., 30: 1%31.
Schultz,A.H. (1926)Fetal growthofmanandotherprimates.
Quart. Rev. Biol., 2:465521.
Schultz, A.H. (1933) Die Korperproportionen der erwachsenen catarrhinen Primaten, mit spezieller Beriicksichtigung der Menschenaffen. Anthrop. Anz.,10:154-185.
Schultz, A.H. (1956) Postembryonic age changes. In:
Primatologia I. Systematik, Phylogenie, Ontogenie.
Karger, Basel, pp. 887-964.
Stem, J.T., Jr. (1971) Functional myology of the hip and
thigh of cebid monkeys and its implications for the evolution of erect posture. Bibliotheca Primatologica, No. 14,
318 pp. S. Karger, Basel.
Stem, J.T., Jr., and C.E. Oxnard (1973) Primate locomotion:
some links with evolution and morphology. Primatologia,
vol. 4, If. 11. Karger, Basel.
Stem, J.T., Jr., J.P. Wells, A.K. Vangor, and J.G. Fleagle
(1977) Electromyography of some muscles of the upper
limb in Ateles and Lagothrix. Yrbk Phys. Anthropo1.i976,20149a507.
Tuttle, R.H., and J.V. Basmajian (1977) Electromyography
of pongid shoulder muscles and hominoid evolution. I. Retractors of the humerus and “rotators” of the scapula.
Yrbk. Phys. Anthropol.-l976,20:491-497.
Tuttle, R.H., and J.V. BasmaJian (1978) Electromyography
of pongid shoulder muscles. 111. Quadrupedal positional
behavior. Am. J. Phys. Anthropol., 49:57-70.
Washburn, S.L. (1963) Behavior and human evolution. In:
Classification and Human Evolution (Viking Fund Publ.
in Anthrop., No. 37). S.L.. Washhum, ed. Wenner-Gren
Found. Anthrop. Res., New York, pp. 190-203.
Документ
Категория
Без категории
Просмотров
0
Размер файла
913 Кб
Теги
major, atelines, clavicular, electromyography, stud, evolution, pectoralis, hylobates, pars, references, special
1/--страниц
Пожаловаться на содержимое документа