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An analysis of the muscular limitation on opposability in seven species of Cercopithecinae.

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An Analysis of the Muscular Limitation on Opposability in
Seven Species of Cercopithecinae
FRANCES D. BURTON
D e p o r t m e n t of A n t h r o p o l o g y , U n i v e r s i t y of Toroltto,
Toronto 5, O n t a r i o , C a n a d a
KEY WORDS
Primates . Musculature . Opposition
. Adaptation.
ABSTRACT
Cercopithecinae have long been considered to have a manus
capable of opposition. Observations of manipulation in seven quadrupedal
species of Cercopithecinae show that three opposable grips are used, ranging
from the ultimate refinement of the "precision grip," the refined opposition,
where contact is made between the distal pads of the first digit (dl) and the
second digit (d2), to the cup, where the pollex is equidistant from, and presses
a n object against, the palmar pads of the other digits. The most frequently used
hand position was the quasi-opposition, where the distal pad of d l contacts d2
anywhere along its lateral aspect.
Dissections of the muscles of the pollex showed that i n all the species studied
refined opposition depends on the abductor brevis and opponens pollicis. In
general the other pollical muscles, which enhance opposition in man, are
limiting factors on this movement.
The differences among the species, however, tend to reflect use of the hand.
Thus, those species subsisting principally on a diet of seeds and grasses were
found to have the highest frequency of refined opposition, and their pollical
anatomy shows a muscular configuration facilitating opposition.
The suggestion is made that manipulation as i n procuring, conveying and
preparing food may have been a more important adaptive pressure than locomotion in retention of the generalized form of the cercopithecine hand.
One of the factors most influencing the
evolution of man has been his ability to
manipulate objects. The phylogenetic development culminating i n this ability has
received relatively little attention. The
majority of studies on the non-human
hand have concentrated on it as a part
of the locomotor complex (e.g., Keith,
1894; Jouffroy and Lessertisseur, '60; Oxnard, '63; Bishop, '64; Tuttle, '67). The
major exceptions include the two papers
by Alison Bishop on the Prosimii ('62,
'64), both behavioral studies, Hall and
Mayer's work on Erythrocebus patas
('66), and the work of J. R. Napier since
1955, which has concentrated on certain aspects of the anatomy of the hand
of non-human primates in general while
including behavioral aspects. The progression from convergent (represented by Tarsier) to prehensile (represented by Callithrix) to pseudo-opposable (represented
by Cebus) to opposable (represented by
Cercopithecoidea, Pongidae and Homo)
AM. J. PHYS. ANTHROP.,36: 1 6 S 1 8 8 .
(Napier, '61; Napier and Napier, '67) has,
according to Napier, led to a hand capable of opposition, and its refinement, the
precision grip.
Opposition is defined as a combination
of movements -flexion, abduction and
conjunct rotation - which rotate the
thumb on its longitudinal axis so that the
palmar surface of the tip of the thumb
comes i n contact with the palmar pads
of the other digits (Duchenne, 1858, cited
in Kaplan, '53; du Bois Reymond, 1895;
Schultz, '26; Haines, '44; LeGros Clark,
'59; Napier, '60; Jones, '67). The ability
to oppose is intrinsic to the cercopithecine
hand due to the carpometacarpal saddle
joint. The degree to which opposable grips
are used, however, varies from species to
species within the taxon.
The limitations on the use of opposition may coincide with two factors: the
type and nature of foods eaten in the wild
1 Editor's Note: The photographs were taken under
field conditions.
169
170
FRANCES D. BURTON
TABLE 1
The three opposable g r i p s of cercopithecines
Grip
Movement
Refined
opposition
Quasiopposition
1
CUP
~~
x
Abduction
Flexion
Conjunct rotation
Adduction
Extension
Relation to
second digit
X
X
X
X
X
X
X
X
Palmar surface of
d l touches palmar
surface of d2.
Palmar surface
d l contacts
side d2 anywhere from j u s t
proximal to the
head of the 1st
phalanx to just
proximal to tip
of distal
phalanx.
Opposes all
digits. Palmar
surface of d l
presses object
equally against
surface of d2d5.
1 Although subsuming precision, this grip is NOT identical to Napier’s “precision grip” (’61, ’66).
since h e does not distinguish between opposition a n d precision. I n h i s precision grip, “The fingers are
slightly flexed at the metacarpophalangeal joint a n d interphalangeal joints. The thumb is abducted,
flexed and medially rotated (opposed position.)” (’66, 26). His figure illustrating the precision grip
(’66, 25, 12b) shows a h a n d holding a round object so that the pad of the thumb is equidistant from the
other digits. While this i s a n opposed grip, it can be accomplished without fine control. Each successive
stage i n the evolution of the primate h a n d h a s a s its correlate increased control of the hand in manipulation. It would seem, then, t h a t refined opposition more properly reflects a refinement i n the efficiency
of opposition.
TABLE 2A
Frequencies and percentages of total obseruations of the three opposable grips
used by cercopithecines on all foods
Frequencies of opposable grips only
C. ascanius
C. mitis
C. neglectus
C. aethiops
E . patas
M . mulatta
P. cynocephalus
C. ascanius
C. mitis
C. neglectus
C . aethiops
E. patas
M . mulatta
P. cynocephalus
Refined
opposition
Quasiopposition
CUP
Total of
all grips
(2,100)
2
14
22
17
36
115
115
110
108
70
62
34
75
84
85
73
28
46
7
350
350
350
350
300
200
200
70
1
159
Percentages 2
0.09
5.48
0.67
5.48
1.05
5.24
0.81
5.14
1.71
3.33
3.33
2.95
7.57
1.62
3.57
4.00
4.05
3.48
1.33
2.19
0.33
1 Grain
2
only.
Opposable grip calculated a s per cent of total observation for all grips
and the disposition of the intrinsic muscles of the thumb. The form of a structure is intimately allied with its function,
and this paper attempts to illustrate this
relationship. Thus, opposition is found
more frequently in those species whose
muscles enhance this movement and
whose survival requires this movement in
order to exploit the nutritive resources
available to it.
171
LIMITATION ON OPPOSABILITY I N CERCOPITHECINAE
TABLE 2B
C o u n t s of grip f r e q u e n c y f o r grain o n l y
RO
Species
QO
CP
F
COB
N-0
N-0
QO
CP
~~
C. nscanius
C. mitis
C. neglectus
C . nethiops
E. patns
M . mitlattu
P. c y n o c e p h a l u s
1
11
1
7
11
35
3
3
1
5
47
38
2
37
15
I
1
8
-
5
1
-
-
I
0
3
7
4
-
METHODS
Research on the use of the hand showed
that cercopithecines use five basic hand
positions of which three are opposable
grips (table 1). Counts were taken on the
frequency with which each grip was used
on ten different foods.2 The foods were
selected because (1) they are foods eaten
in the wild by most of the species studied and (2) the size, shape and nature of
the covering of each of them presented
a specific problem i n manipulating and
conveying the food to the mouth. Grain
(i.e., oats) was found to be the best discriminant of precision usage as it is
small (1 cm) and its smooth husk and
oval shape require the finest control. Two
grips only were used in manipulating and
conveying this food to the mouth: the
refined opposition and the quasi-opposition grips (table 1). Fifty observations per
food per species were made. Frequencies
and percentages of total observations per
species are given i n table 2A and counts
of grip frequency for grain only are given
in table 2B.
The species (table 3 ) were chosen (1)
for their availability and (2) in terms of
a “ground-to-tree gradient.” Thus, Cercopithecus ascanius, 3 C. mitis, C. neglectus, C. aethiops, and Erythrocebus patas 4
were studied in family groups housed in
large cages, measuring 12’ X 8’ X 8’, at
Tigoni Primate Research Centre in 1966.
The cages were large enough to permit
free locomotion and manipulation i n a
social setting. A variety of foods were fed,
being placed on the concrete floors of the
cages. Macaca mulatta and Papio cynocepkalus were studied at Primate Centers in the United States i n 1967 and
1968. They were housed in single cages
not exceeding 35“ wide, by 35” deep, by
48” or 54” high and were fed monkey
-
-
-
-
-
-
-
-
-
-
-
-
-
7
-
-
1
9
1
-
-
-
-
-
-
-
-
-
-
-
-
F
~
-
chow from a hopper that was supplemented with fruits and vegetables at one
of the Centers (Holloman). Table 4 gives
the natural habitats and table 5 gives
the natural diets for these species as recorded in the literature.
Thirty-eight animals were dissected in
Africa at Tigoni Primate Center and at
Primate Centers in the United States
(table 6). Dissections were made of fresh
or frozen specimens.
RESULTS
The frequency counts of hand positions
confirmed Napier’s (‘67) suggestion that
the use of precision coincides with terrestrial adaptation as P. cynocephalus showed
frequencies of refined opposition higher
than all the other species, and E. patas
had frequencies higher than all the Cer2 These foods included: greens, carrots (Daucus carota), potatoes, maize (Zea mays), yellow-skinned bananas, mango (Mangifera), grain (oats Avena satlva),
pineapple (Ananas comosus), chow-chows (Pachystela
brevipes) and granadilla (passion-fruit, Passiflora cere).
For M. mulatta, studied at Primate Centers i n the
United States, apple, banana and monkey-chow bits
approx. 1 cm in size were substituted because of their
availability. The primary problem presented by pineapple and chow-chow (both fed i n lengthwise slices),
carrots and potatoes, is their size. Granadilla, mango
and banana have shells or skins, and these h a d to be
broken or peeled. Lettuce a n d greens are limp a n d were
awkward to handle. Maize and grain presented the most
formidable problems, the former because strength was
required both to remove the husk and support the ear,
and the latter, because its small size (each kernel
approximately 1 cm long), oval shape a n d smooth husk
necessitated the finest control. Fifty trials per food
were given each species, except for M. mulatta and
P. cynocephalus whose normal diets precluded their
introduction.
3 C. ascanius refers to the East African red-tail
guenons (Hill, ’66:489), placed within the superspecies
C. petaurista ( [ b i d . : 474). The species is grouped with
the West African spot-nosed guenons, C. nictitans i n
the “Nictitans group” by Napier (’67).
4 Discussions concerning the placement of this genus
within Cercopithecus have gone on for some time (see
Hall and Mayer, ’66). This study follows the work of
Hall and Mayer (’66) i n retaining the generic n a m e
Eryt hrocebus.
172
FRANCES D. BURTON
TABLE 3
Living cercopithecines observed for hand grips
Sixmes
C. mitis
C. neglectus
C. nethiops
C. ascnnius
E . patns
M . mulntta
Holloman
Delta
P . cynocephalus
Delta
Adult
females
Adult
males
Sub a d d t
males
13
9
6
2
6
9
5
5
1
3
2
2
1
Subadult
females
Total
27
17
13
4
6
-
-
4
3
6
-
14
1
2
3
-
5
86
Total
TABLE 4
Habitat of the cercopithecine species studied a s reported i n the literature
C.
ascanius
Tropical forest
Gallery forest
Montane forest
Sparser forest
Woodland
Swamp
Savanna
C.
niitis
C.
neglectus
X
X
X
X
X
X
X
X
X
X
x (?I
C.
aethiops
E.
patas
P.
cynocephalus
M.
niiilatta
x (Ethiopia)
X
X
X
X
X
X
X
X
X
X
X
NOTE: Field reports a s follows:
C. ascanizcs-Haddow, '52.
C. mitis-Haddow, '52; Booth, '62; Tappen, '60, Gartlan and Brain, '68.
C. neglectus-Booth, '62, '68; Hill, '66; Haddow, '52.
C . aethiops-Struhsaker, '67; Hall and Gartlan, '65.
E. patns-Hall, '66.
P. cynocephalus-DeVore a n d Hall, '65; DeVore and Washburn, '63.
M. mzclattcz-Southwick et al., '65.
copithecus species. Species like M. mulatta and C. aethiops, however, which spend
part of their time on the ground, confound the issue. M. mulatta showed frequencies of the refined opposition grip
that were higher than the terrestrially
adapted E. patas. C. aethiops had frequencies lower than C. neglectus, which
spend less time on the ground. These animals are all classified in terms of locomotion as quadrupeds (Oxnard, '63; Napier
and Napier, '67) with specializations in
cheiridia attributed to the place of locomotion (e.g., E . patas, Hall, '62; Oxnard, '63; Hall and Mayer, '66). The
cercopithecine hand is considered to have
remained a generalized organ (Midlo, '34;
Romer, '66), as contrasted with the prosimians (Bishop, '62, '64) or pongids (Tuttle, '67). The discrepancies i n a n otherwise clear-cut ground-tree gradient in
frequency count of hand position used
suggest that some factor other than or in
addition to locomotion, such as manipulation, may have been influential as a n
adaptive influence in Cercopithecinae.
Napier has shown that two factors are
critical i n modifying the ability to oppose
in Cercopithecinae: (1) the length of the
thumb measured against the length of
the second digit a s reflected in the opposability index (Napier and Napier, '67), and
(2) the degree of curvature of the carpal
canal (Napier, '61). The present research
indicates that a third factor, the musculature of the thumb (the critical digit in
opposition) is a further limitation on opposition.
The carpometacarpal saddle joint of the
thumb permits flexion, extension, and abduction (Haines, '44). Conjunct rotation
(MacConaill, '46), a movement essential
173
LIMITATION ON OPPOSABILITY IN CERCOPITHECINAE
TABLE 5
Diet of the cercopithecine species studied a s recorded infield reports
C.
C.
C.
C.
E.
ascanius
initis
neglectus
aethiops
patas
X
X
X
X
Tree
Leaf
Leaf bud
Flower
Roots
Cultivated crops
Fruits
Grasses
Seeds
Berries
Meat
Vertebrate
Invertebrate
Pods
Beans
M.
P.
cynocephalus
niulatta
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
NOTE: Field reports as follows:
C. ascanius-Haddow, '52.
C. mitis-Booth, '62, '68.
C. neglectus-Booth, '62.
C. aethiops-Struhsaker, '67.
E. pata-Hall, '66.
P. cynocephalus-DeVore and Hall, '65; DeVore and Washburn, '63.
M.mulatta-Southwick, '66; Southwick et al., '65; Neville, '68.
TABLE 6
Dissected cercopithecine specimens
Center
Species
Tigoni
C.aethiops
C. neglectus
M
F
M
4
3
F
1
Holloman
Delta
Total
1
9
1
3
2
(no specimens available)
C.ascanius
C.mitis
M
F
5
2
E . patas
M
F
2
2
M . mulatta
M
F
P. cynocephalus
M
F
Totals
LEMSIP
M
19
19
to opposition, is actually a derivative of
these, as rotation first involves flexion of
the metacarpal and then abduction of it
(Napier, '66). The form of this joint in
man and Cercopithecinae permits their
manipulative abilities. Indeed, it is the
rotation of the metacarpal which accord-
7
2
3
2
6
1
8
2
2
1
2
5
38
ing to Napier ('61) defines true opposition in the Catarrhini as differentiated
from pseudo-opposition in Ceboidea.
The metacarpophalangeal joint of the
thumb, a hinge type of joint, permits
broad movement: abduction, adduction,
flexion, extension and some axial rota-
174
FRANCES D. BURTON
tion. Because abduction and rotation are
permitted at this joint, it is responsible
for opposition as well (Napier, ’66).
The interphalangeal joint of the thumb
permits only flexion and extension. Stability is critical to opposition, which requires
a steady pressure on a n object, so that
the placement of the two muscles that
principally work over the joint is most
important.
The myological variations found tend
to correlate with the observations of grip
frequency. These variations include: (1)
all species differing from one another,
and (2) some species clustering, but collectively differing from the remaining
species.
A. Carpometacarpal joint of the t h u m b
The complex of movements permitted at
this joint are brought about by four muscles: the abductores longus et brevis, the
opponens pollicis and the flexor pollicis
brevis (plates 1-5).
The opponens pollicis, i n all species of
Cercopithecinae studied, originates from
the flexor retinaculum and the ridge of
the trapezium and scaphoid and inserts
on the medial to radial aspect of the head
of the metacarpal.
A slight variation was found in C. neglectus, where the opponens receives a
tendon from the abductor longus-extensor
brevis complex. The addition of these
fibers may be a partial explanation for
the ease with which C. neglectus assumes
the refined opposition grip, as their exertion conjointly with the opponens would
enhance stability of the metacarpal, and
so increase abduction that opposition
would be facilitated. The insertion for
C. neglectus is quite similar to that described for the other Cercopithecus species, except that the opponens belly is
more pronounced, bunched proximally,
and sends a long thin tendon to the insertion. The muscle is very slim in C. mitis
and C. aethiops, appearing almost translucent.
The muscle has the same origin and insertion in E . patas (fig. 1) as i n Cercopithecus (fig. 4). The specimens of P . cynocephalus (fig. 2) and M . mulatta (fig. 3 )
show a similar pattern: the opponens,
running deep to the abductor brevis and
flexor pollicis brevis, as it does in all cercopithecine species, takes origin from the
flexor retinaculum and trapezium, with
some fibers occasionally from the scaphoid, and inserting on the head of the
metacarpal, towards the lateral aspect.
In P. cynocephalus, the muscle attaches
along the length of the metacarpal, perhaps thus gaining more mechanical advantage.
Day and Napier (‘63) have discussed
the phylogenetic significance of the deep
head of the flexor brevis and have found
it to exist in Cercopithecoidea, being especially well developed in M . mulatta. They
noted the probable phylogenetic migration
of the deep head from a n attachment
on the ulnar sesamoid to a n attachment
on the radial sesamoid and remarked that
this migration seemed related to the “acquisition of true opposability in catarrhines” (‘63:122). In the specimens of
Cercopithecinae studied, there seems to
be great variation in this muscle, even
between the two upper extremities of one
579). The two
animal ( M . mulatta,
heads of the flexor brevis are most clearly
defined in the specimens of P. cynocephalus and least clearly in Cercopithecus spp.
Where there are two heads present, the
superficial head takes origin from the
retinaculum and trapezium, and the more
medial deep head takes origin from the
flexor retinaculum and trapezoid ( P . cynocephalus, M . mulatta, E . patas, C. neglectus). Both heads insert on the proximal
phalanx, the medial head attaching to
the head of the metacarpal as well. The
fibers of the two heads are often found
to be intertwined (P. cynocephalus, M .
mulatta and E . patas), and sometimes
only one head is discernible (C. mitis,
C. aethiops, C. neglectus, E . patas, M .
mu la t ta).
The abductor brevis, whose principal
actions are on the proximal phalanx of
the thumb (Wood Jones, ’ZO), has generally been considered to be most responsible for opposition (Wood Jones, ’20;
Napier, ’52; McFarlane, ’62). The abductor brevis showed little variation in all the
species of Cercopithecinae studied. It takes
origin from the flexor retinaculum, the
tubercle of the scaphoid and the crest
of the trapezium, and inserts on the lateral base of the proximal phalanx with
LIMITATION ON OPPOSABILITY I N CERCOPITHECINAE
fibers moving into the dorsal expansion.
Differences between origin on both scaphoid and trapezium occur, but as these are
equally within species as between species
they do not seem significant.
The abductor pollicis longus is known
in the earlier literature as the extensor
ossis metacarpal pollicis (Primrose, 1899;
Wood Jones, ’20; Straus, ’41) and has
been considered homologous with the supinator manus of reptiles and amphibians
(Straus, ’41).
The abductor pollicis longus cannot be
discussed in non-human primates without reference to the extensor pollicis brevis. Most authorities maintain that there
is no extensor pollicis brevis in catarrhini
(Polak, ’08; Jouffroy and Lessertisseur,
’60), although Straus (‘41), who subscribed to this view, also noted that i t is
occasionally found in gibbons and gorillas.
Wood Jones stated that rather than seeing the extensor pollicis brevis as new in
higher catarrhini, including man, it is
more correct to say that separation of the
extensor pollicis brevis from the abductor
pollicis longus is fully realized in man.
This latter view was substantiated in the
dissection of 38 specimens of Cercopithecinae where it was found that there is a
tendency towards separation of the extensor in some of the species. In the present
study the degree of separation was found
to coincide with higher frequency of the
refined opposition grip.
The abductor pollicis longus and the
extensor pollicis brevis form a muscular
complex (plates 3-5). They take origin
as one muscle, or as two very much
joined. They insert as a unit even when
the fibers of the two can be distinguished.
In general, the abductor-extensor complex
takes origin high on the posterior surface
of the forearm, between the radius and
ulna, with the abductor portion more
proximal. The complex then passes down
the forearm, usually attaching onto the
dorsum of the trapezium, the radial side
of the base of the metacarpal of the
thumb, and on into the flexor retinaculum
on the ventral side of the hand. When
the fibers can be separated, slips or fibers
of both abductor and extensor insert onto
the base of the metacarpal, trapezium,
sesamoid and the flexor retinaculum. All
175
the species do not have all the attachments as discussed below. A designation
at the carpal-metacarpal region of fibers
as abductor or extensor is made. The
fibers and tendon deriving from the radial portion of the mass on the forearm
were termed “extensor,” while those from
the u l n a portion of the mass were termed
“abductor.”
In C. mitis, although the extensor is so
fused with the abductor that the fibers
could not be separated, the extensor portion of the joint tendon could be demarcated. The two tendons insert as an intertwined unit onto the sesamoid and base
of the metacarpal and the trapezium, but
the extensor portion remains a visible
entity.
In C. aethiops (fig. 5), the abductor pollicis longus and extensor pollicis brevis
are separate at their origin. The abductor
crosses over the extensor and joins with
it to form a tendon which inserts on the
sesamoid and retinaculum and the base
of the metacarpal to form the base of a
triangle. The extensor portion is again
separable from the abductor and inserts
onto the trapezium, across to the base
of the metacarpal, and onto the sesamoid
and retinaculum. In C. neglectus as in
C . aethiops, the tendons coming from the
joint mass insert as one but can be separated. The abductor lies lateral to the
extensor and can be seen as a distinct
tendinous portion slightly above the carpals. It inserts on the lateral, almost
ventral side of the base of the metacarpal.
Some fibers attach onto the sesamoid and
retinaculum, and some fibers onto the
opponens pollicis. The extensor inserts by
a minor slip onto the trapezium, and then
passes a major slip over to the base of the
metacarpal, sesamoid and retinaculum,
inserting underneath the abductor.
E . patas (fig. 6 ) is somewhat different
in the insertion of abductor longus. A
major slip from the abductor inserts onto
the sesamoid and retinaculum, and a
major slip from the extensor inserts onto
the base of the metacarpal. A secondary,
minor slip emerges from the major tendons. The extensor portion inserts on the
sesamoid and retinaculum, and the abductor portion on the metacarpal distal
to the insertion of the extensor. There
seems to be no attachment onto the trape-
176
FRANCES D. BURTON
zium. As with C. aethiops, there is a
separate origin for each muscle.
While the high refined opposition performance in P. cynocephalus (fig. 7 )
seems to suggest a further development
of separate muscles, this expectation was
not confirmed at dissection. The muscle
mass takes origin high on the ulna and,
immediately crossing to the radius, descends in the forearm. The tendon inserts
as one unit a s the base of a triangle,
whose left leg, the abductor portion, attaches to the sesamoid and the trapezium.
The tendon could be separated at the
level of the carpal end of the radius, but
neither the muscle fibers nor the inserting tendon could be separated.
The muscles of the M. mulatta (fig. 8)
specimens are like P. cynocephalus in origin, but rather more like C. aethiops and
C . neglectus in insertion. At the base of
the muscle belly, approximately 2 mm
from the carpals, two tendons are separable. The abductor portion inserts on the
sesamoid and trapezium, and the extensor portion on the base of the metacarpal,
but the two tendons insert as one triangular piece.
In tenns of opposition, the differences
in origin and insertion of the abductorextensor complex are significant. When
the extensor brevis is functionally totally lacking (C. mitis), the actions of this
muscle are, of course, not available.
Where the extensor exists as independent
tendinous fibers only a t insertion ( M .
mulatta, C. neglectus), and otherwise
closely intertwine with abductor fibers,
contraction of the abductor triggers the
extensor fibers to act and, from their
attachment on the radial side of the base
of the metacarpal, extend dorsally and
slightly abduct the metacarpal. The separate abductor portion of the common
insertion on the carpal acts as a n abductor of the hand, although in those animals where there is a metacarpal insertion as well (C. neglectus, C. aetkiops,
E . patus) the abductor portion can aid in
stabilizing the metacarpal. The configuration of the complex in C. aethiops and
E. patas is similar: separate origin and
separate insertion of the two masses.
However, as the extensor brevis does not
insert on the base of the proximal phalanx, opposition in these animals must
also be more difficult to attain, since
stability of the metacarpophalangeal joint
can only be achieved by residual effort
of the intrinsic muscles inserting into the
dorsal expansion. Furthermore, since the
abductor attaches most consistently to the
trapezium and sesamoid, rather than to
the metacarpal itself, stability at the
carpometacarpal joint is curtailed, and
abduction from the action of this muscle
is minimal.
B . Metacarpophalangeal joint of
the t h u m b
Movement at this joint -flexion, extension, abduction, adduction, and axial rotation - are fundamental to the movement of opposition, as the medial twisting
of the proximal phalanx results in functional rotation of the digit. The muscles
involved are the abductor pollicis brevis,
flexor pollicis brevis, extensor pollicis brevis and adductor pollicis. The first three
muscles have been discussed in the preceding section, as they either act over the
carpometacarpal joint (abductor brevis,
flexor brevis) or relate to a muscle that
does (extensor brevis).
The adductor pollicis acts on the metacarpophalangeal joint to draw the digit
to the palm of the hand. The function of
the adductor pollicis in opposition is to
stabilize the thumb (Napier, '66). Force
exerted by the second digit is counteracted at the metacarpophalangeal joint
so that the head of the metacarpal and
the base of the phalanx are firm.
The origin of both the transverse and
oblique portions of the adductor is the
same in all the Cercopithecinae studied.
The heads of the adductor insert separately but with minor variations. In C.
aethiops the transverse head inserts from
the head of the metacarpal to the base of
the proximal phalanx, and the oblique
head inserts on the lateral aspect of the
head of the metacarpal. The insertion of
both of these is similar in C. mitis, but
the oblique is a stouter muscle than it
is in C. aethiops.
The insertion of these two parts of the
adductor i n E . patas and C . neglectus is
on the lateral aspect of the head of the
pollical metacarpal, and the transverse is
a very thin muscle. In C. neglectus it is
LIMITATION O N OPPOSABILITY IN CERCOPITHECINAE
still visible as a muscle, but in E . patas,
i t merely consists of muscle fibers in con-
nective tissue. In M. mulntta, the transverse head attaches more distally on the
metacarpal shaft than does the oblique:
from the middle of the metacarpal shaft
to the base of the first phalanx. The
oblique attaches to the head of the metacarpal and the base of the first phalanx.
P. cynocephalus differs from the other
species described in that the distance
between the two heads of the adductor
is very great. The transverse head inserts
on the metacarpal and onto the medial
aspect of the base of the first phalanx
while the oblique head inserts on the head
of the metacarpal and into the insertion
of the transverse.
There is a strong correspondence between the weakness or slimness of the
transverse head of the adductor and high
refined opposition performance. In Cercopithecus species aethiops and neglectus,
whose performance is markedly higher
than that of C. mitis or C. ascanius, the
transverse head, i n comparison to the
oblique, is extremely poorly developed.
This is also the case in E . patas, where
the transverse is so reduced as to appear
merely as isolated fibers with a connective tissue matrix. In P. cynocephalus,
the two heads are distinct from each
other, appearing more as separate muscles than as two heads of the same
muscle. The oblique head is better developed than the transverse head.
C . lnterphalangeal joint of
the t h u m b
There are only two muscles that work
across this joint whose role in opposition
is very important. These are the flexor
pollicis longus (plates 6, 7) and the extensor pollicis longus. The extensor pollicis longus is a “real muscle i n principle”
in primates (Jouffroy and Lessertisseur,
’60:128). Its origin is on the posterior
aspect of the ulna and adjacent interosseous membrane distal to the abductor
longus in all species studied. The insertion for all species is into the base of the
distal phalanx.
The extensor pollicis longus extends
the distal phalanx of the thumb, and
pulls the entire digit dorsad. It is a n
177
antagonist to the opponens pollicis (Wood
Jones, ’20), as it can rotate the thumb
dorsally. Its primary function is to exert
a counterforce against the flexor pollicis
longus. When these two muscles act, they
stabilize the interphalangeal joint and
maintain the distal phalanx.
In Cercopithecinae, the flexor pollicis
longus arises as a tendon from the flexor
digitorum profundus mass. Its degree of
independence from the mass does vary.
In E . patns (fig. 9), this separation is
considerably more proximal than it is in
the Cercopithecus species, coming from
the flexor digitorum profundus a t the carpals rather than from the palm. This origin is also found in M. mulatta (fig. lo),
but not in P. cynocephalus (fig. ll), where
the flexor pollicis longus takes origin more
proximal than the carpa1s.
The separation of the flexor pollicis
longus a t the palm for Cercopithecus species is generally from the center of the
flexor digitorum profundus, or slightly
radial (fig. 12), although i n two specimens of C. aethiops, it came from the
ulnar side.
The terminal insertion of this muscle
is the same for all specimens of Cercopithecinae studied, i.e., at the very tip of
the distal phalanx.
The flexor pollicis longus works i n direct opposition to the extensor pollicis
longus. It flexes the terminal joint of the
thumb and has a limited effect on the
proximal joint as well. In opposition when
the palmar pad of the distal phalanx of
the thumb contacts the distal palmar pad
of the second digit, the exertion of the
flexor longus stabilizes the terminal phalanx a t the interphalangeal joint, and
thus permits manipulation of a n object
(Napier, ’66; Kaplan, ’65). When the
thumb has moved into a position of opposition, but is not contacting the second
digit, it is the mutual exertions of the two
long muscles that hold the terminal phalanx firm. The insertion of the flexor
pollicis longus into the tip of the distal
phalanx in all the Cercopithecinae studied results in loss of control of the interphalangeal joint.
This reduction in efficiency is due to
the fact that contraction along the flexor
pollicis longus is not counterbalanced by
the contraction of the extensor pollicis
178
FRANCES D. BURTON
longus. As the counterforce exerted by
the extensor longus is to the base of the
distal phalanx and not the tip, there is
no means of inhibiting this action of the
flexor. That this does occur is observed
in the variation of the quasi-opposition
grip where the ungular surface of the
thumb is pressed against the side of d2.
DISCUSSION
None of the species studied was observed to approach 100% refined opposition use with food items of small size and
smooth texture. Yet opposition is intrinsic
to the cercopithecine hand.
All of these species have the same number of pollical muscles. Where the pattern
of origin or insertion of the muscles was
the same for all species, that pattern was
taken as a n absolute limitation on opposition in every species studied as compared to man. The elements of this pattern include: (1) the insertion of the
flexor pollicis longus; and ( 2 ) the insertion of the abductor pollicis longus-extensor pollicis brevis complex.
For all species studied, the flexor pollicis longus inserts at the distal end of
the distal phalanx. As its antagonist, the
extensor pollicis longus, inserts at the
base of the distal phalanx, there cannot
be counterforce exerted against its action.
Clinical studies of H . sapiens have
shown that such a pattern results in loss
of stability of the interphalangeal joint,
and consequent loss of control of the
digit in precision grips (Kaplan, '65). This
observation reinforces the view that the
distal insertion of the flexor pollicis longus
inclines the species studied to press the
terminal phalanx of the pollex against the
side of the second digit where stability
at the interphalangeal joint is enhanced.
The abductor pollicis longus-extensor
pollicis brevis complex inserts i n all Cercopithecinae studied on the base of the
metacarpal, the trapezium and the sesamoid, with some variation in C. neglectus.
In H. sapiens, not only does the complex consist of two independent muscles
from origin to insertion, but insertion
extends more distally on the pollex, the
abductor inserting on the metacarpal and
the extensor onto the proximal phalanx.
The proximal insertion of the complex in
Cercopithecinae seems to make it function as a n extensor ossis metacarpal pollicis or supinator manus, so that working
across the carpometacarpal joint the digit
is pulled dorsad, and is only slightly abducted. Furthermore, extension of the
digit occurs primarily at the distal phalanx, with some action across the carpometacarpal joint, but not over the metacarpophalangeal joint, and abduction is
basically limited to the activity of the
abductor pollicis brevis.
As abduction is a primary movement in
the total act of opposition, its decrease
through the absence of a functional abductor longus limits the ability to oppose.
This fact has been confirmed for H. sapiens i n clinical studies (Napier, '52).
Variation in observed manipulative behavior of the several species of Cercopithecinae suggests anatomical differences between them. Those myological
factors which were observed to vary between species are judged to be the critical
variables. These include: (1) the origin
of the flexor pollicis longus, ( 2 ) the insertion of the abductor-extensor complex,
and (3) the transverse head of the adductor.
The origin of the flexor pollicis longus
varies in degree of independence from
the flexor digitorum profundus. i t takes
origin at the carpals, proximal to the
carpals, or distal to the carpals. As those
species with the highest refined opposition performance have the most proximal
origin of the flexor pollicis longus (P.
cynocephalus, M. mulatta, E . patas), it
was deduced that the greater resulting
length of the flexor must permit greater
independence i n flexion of the pollex from
the other digits. The greater independence
would permit manipulation in relation to
the other digits (as in opposition) rather
than synergistically with the other digits.
The intimate relation of the abductor
to the extensor i n a muscular complex
results in its acting as a n extensor of the
metacarpal or radial abductor of the hand,
as noted above. However, the degree of
independence of the abductor longus from
the extensor brevis at origin and insertion
varies between species. The greater the
independence, the higher the frequency
of refined opposition. With insertion on
the metacarpal and fibers anchored on
LIMITATION ON OPPOSABILITY I N CERCOPITHECINAE
the sesamoid andlor trapezium, contraction principally results i n motion dorsad
but some abduction, mediated by the more
volar fibers, is permitted.
The degree of independence correlates
with manipulative behavior except i n P.
cynocephalus subjects where the muscular
configuration of the complex is more like
the species with lower frequency count>
of refined opposition. But even here, while
the origin and insertion of the two muscle entities are as one mass, the tendon
is separable a t the carpals before intertwining at insertion. Significantly, P. cynocephalus has the greatest degree of
carpal curvature of cercopithecines (Napier, '61). As a complex of variables and
not a single factor must account for manipulative behavior, perhaps the reduced
distance between the pollex and the second digit, due to the curvature of the
carpus, compensates for the configuration
of the abductor-extensor complex i n this
species.
The adductor pollicis functions i n opposition to stabilize the metacarpophalangeal joint (Napier, '66). It also works as
the antagonist to the abductor-extensor
complex (Wood Jones, 'ZO), drawing the
pollex medially towards the second digit.
The transverse head is considerably thinner-even
to the point of appearing as
fibers only -in those species with highest refined opposition performance. This
fact suggests that i n these species ( P . cynocephalus, M . mulatta, E . patas, C.
aethiops, C. neglectus) stability of the
metacarpophalangeal joint is maintained
by the oblique head, but the action of
drawing the thumb medially is reduced.
In species deriving a small degree of abduction from the abductor longus, as in
all the species studied, a weak transverse
head facilitates abduction by reducing
counterforce, thus permitting greater opposition.
Refined opposition in the species of Cercopithecinae studied depends on the abductor brevis and opponens pollicis. The
other pollical muscles, which enhance
opposition in H . sapiens, are limiting factors in these species.
While all the factors leading to the
observable differences in performance are
not yet clear, there is a superficial correspondence between the diet which the
179
habitat affords and the frequency of refined opposition. It is phylogenetically significant that those species inhabiting
savanna and therefore subsisting principally on seeds and grasses ( E . patas, P.
cynocephalus) have a very high frequency count of refined opposition grip.
The gallery forest dwellers, who occasionally descend to the substrate (C. neglectus), are similar to the committed
ground dwellers in certain anatomical
features, particularly the abductor-extensor complex and the transverse head of
the adductor. This is reflected in the
refined opposition performance. However,
the data concerning their feeding habits
are largely anecdotal, and the degree to
which they exploit the food resources of
the substrate must await future reports.
On the basis of their manipulative behavior and anatomy, a prediction is warranted that some of the foods on which
they depend will be like those of C. aethiops or E . patas, i.e., seeds, grasses or the
like.
The diet of tree dwellers (C. ascanius
and C. mztis) comprises food items that
can be handled with grips of the whole
hand (fruits), such as the cup, or just
the digits d 2 4 5 (leaves). The high quasiopposition frequency observed on food
items such as grain coincides with the
field reports of diets which lack similar
food items.
The non-human primate hand has a
dual function: one is manipulation, the
other locomotion. While it may be true for
Prosimii and Pongidae that the hand has
adapted for locomotion and that its manipulative abilities are a result of the
locomotor adaptation (Bishop, '62, '64;
Tuttle, '67, 'SS), the fact that the cercopithecine hand is generalized (Midlo, '34 ;
Romer, '66) permits a more particular
adaptation for acts of manipulation.
Napier ('62, '66) and Napier and Napier
('67) stress the significance of the strata
of the forest occupied by a given species
as influencing adaptations in the extremities. They agree with Avis ('62) that
the thickness of tree branches as well as
the angle in which they lie relative to the
trunk has been influential in the evolution of the locomotor systems of the various species and their concomitant behavioral development. Admitting that the
180
FRANCES D. BURTON
distribution and density of foods are involved in stratification, they nevertheless
place greater emphasis on getting to the
food than getting the food from its source
into the animal’s mouth:
“The maximum density of fruit a n d
leaves thus tends to be sited peripherally;
i n order to reach a n d feed on the leaves,
the animal is forced to move far out from
the trunk into a milieu that is largely composed of small flexible branches; in such a
setting the suspensory activities of the
hands, feet . , . are called into play.” (Napier a n d Napier, ’67:384).
The nature of the food itself requires
morphological adaptations, as is consistently apparent in dental morphology
(e.g., Jolly, ’70). Quantified analyses of
foods and the frequency of their ingestion
have been made by Haddow (‘52) and
Struhsaker (‘67) for C. asccznius and C.
aethiops respectively. Similar detailed information does not exist for the other
species under consideration. Anatomical
and behavioral observations with caged
animals give some insight into the f a d i t y with which certain foods are manipulated; when the facility of manipulation
coincides with the availability of that
food in the wild, an adaptive tendency
may be located.
ACKNOWLEDGMENTS
I wish to express my appreciation to
Dr. L S. B. Leakey for making my stay in
Kenya possible and for his comments on
the research. I should like to thank Dr.
A. Riopelle, then Director of Delta Regional Primate Center, for his help and
administration of NIH grant FR-00164,
which made my studies in Kenya possible, and for his help in arranging the
research conducted at Delta. Special
thanks is owed to Cynthia Booth, then
Director of Tigoni Primate Research Centre, for her comments and guidance. I am
in debt to Dr. Clyde Kratochvil, Commander of Holloman Air Force Base; Dr.
Jan Moor-Jankowski, Director of LEMSIP;
Dr. T. C. Ruch, Director, and Dr. Daris
Swindler of the Regional Primate Center
of the University of Washington for having made possible research at their respective primate centers. Dr. Ralph Holloway, Dr. John Napier, Dr. Helmut Hofer
and Mario Bick read this manuscript at
various stages and in various forms, and
I a m deeply thankful for their cogent and
considered criticisms. John Glover did the
photographic work. I a m very grateful to
Mrs. Patricia Tiberius for her assistance
in preparation of this manuscript.
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LIMITATION ON OPPOSABILITY IN C E R C O P I T H E C I N A E
Frances D. Burton
EXPLANATION OF F I G U R E S
Flexor brevis, (5);opponens pollicis, (4); abductor brevis, (3).
182
1
E . pntrcs.
2
P. cynocephalus.
PLATE 1
LIMITATION ON OPPOSABILITY IN CERCOPITHECINAE
Frances D. Burton
PLATE 2
EXPLANATION OF FIGURES
Flexor brevis, (5); opponens pollicis, (4); abductor brevis, (3).
3
M.
4
C. riethiops.
nzii/rittLi.
183
LIMITATION O N OPPOSABILITY I N CERCOPITHECINAE
Frances D. Burton
EXPLANATION O F F I G U R E
Abductor-extensor complex, (2).
5
1a4
C. nethiops.
PLATE 3
LIMITATION ON OPPOSABILITY I N CERCOPITHECINAE
Frances D. Burton
PLATE 4
EXPLANATION O F FIGURES
Abductor-extensor complex, (2).
6
E . pntus.
7
P. cynocephnlzis.
185
LIMITATION O N OPPOSABILITY IN CERCOPITHECINAE
Frances D. Burton
EXPLANATION O F F I G U R E
Abductor-extensor complex, (2)
8
186
M . mulutta.
PLATE 5
LIMITATION O N OPPOSABlLITY I N CERCOPITHECINAE
Frances D. Burton
PLATE 6
EXPLANATION O F FIGURES
Flexor pollicis longus, (1).
9
10
E . putus.
M . muluttci.
187
LIMITATION ON OPPOSABILITY IN CERCOPITHECINAE
Frances D. Burton
EXPLANATION OF FIGURES
Flexor pollicis longus, (1)
188
11
P . cynocephnlzrs.
12
C. aet h i ops .
PLATE 7
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species, opposability, seven, cercopithecid, analysis, limitations, muscular
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