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Effects of ontogeny and sexual dimorphism on scapula morphology in the mountain gorilla (Gorilla gorilla beringel).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 98:431445 (1995)
Effects of Ontogeny and Sexual Dimorphism on Scapula
Morphology in the Mountain Gorilla (Gorilla gorilla beringel)
ANDREA B. TAYL,OR
School of Physical Therapy, Sltppery Rock University, Slippery Rock,
Pennsylvania 16057
KEY WORDS
Mountain gorilla, Scapula, Ontogeny, Allometry
Locomotion, Sexual Dimorphism
ABSTRACT
Scapular measurements were obtained from growth series of
the sexually dimorphic mountain gorilla (Gorilla gorilla beringei). Juveniles,
subadults, and adults were compared to determine if scapula morphology
varies with age. Analyses reveal significant (P < 0.05) differences in scapula
form for shape ratios of length vs. breadth, length vs. infraspinous fossa
length, and length vs. spine length. Males and females were also compared
to determine if sexual dimorphism in scapula morphology is a consequence
of differential extension of common patterns of relative growth. Analyses
reveal that scapula proportions are ontogenetically scaled. Data indicate t h a t
male scapulae grow a t a faster rate and for a longer duration than females.
Results of comparisons of males and females suggest that unique adaptations
to different ecological niches have not evolved between the sexes despite
sexual differences in frequency of patterns of locomotor behavior. By contrast,
age-related variation in scapula morphology may be linked to differences in
locomotor behavior during ontogeny. 0 1995 Wiley-Liss, Inc
Gorillas are the largest and most sexually
dimorphic of the extant hominoid primates.
Males weigh approximately 200kg, and females average around 90kg (Fleagle, 1988).
I n addition to being sexually dimorphic in
body size, field studies of the mountain gorilla (G.g. beringei) have documented sexual
differences in frequency of locomotor behavior between adults and patterns of variation
in locomotion as a function of agelsize
(Schaller, 1963; Tuttle and Watts, 1985). Although there may be sexual and ontogenetic
differences in skeletal morphology a s a function of locomotor behavior in mountain gorillas, differences between sexes in adult morphology are best understood in the context
of ontogenetic data since divergence between
sexes can be achieved in numerous ways.
Therefore, patterns of size variation are often explored allometrically utilizing ontogenetic series because such analyses provide
insights into processes of growth and devel0 1995 WILEY-LISS, INC.
opment which underlie differences in size.
Indeed, many analyses of adult postcranial
morphology have revealed that sex differences in adult form are really the products
of differential extension of common patterns
of relative growth (Shea, 1981, 1984, 1992;
Jungers and Susman, 1984; Inouye, 1992;
Jungers and Cole, 1992; Ravosa et al., 1993).
Behavioral studies firmly establish the
dominant mode of locomotion in gorillas to
be a specific form of quadrupedalism known
as terrestrial knuckle-walking (Yerkes and
Yerkes, 1929; Schaller, 1963, 1965; Tuttle
and Watts, 1985). Although not unique
among large-bodied hominoids, gorillas and
chimpanzees share a peculiar form of
knuckle-walking that differs from that of the
orang-utans. In particular, the African apes
Received June 20, 1994; accepted June 2, 1995.
Address reprint requests to Andrea B. Taylor, School of Physi-
cal Therapy, Slippery Rock University, Slippery Rock, PA 16057.
432
A.B. TAYLOR
share a suite of morphological features
which includes marked shortening of the
long digital flexor tendons, tightly packed
articular joint surfaces a t the metacarpophalangeal joints, extremely strong ligaments and tendons in the hand, and specialized pads over the knuckles (Tuttle, 1967).
Together, these features provide for special
weight-bearing adaptations on the dorsal aspects of the middle phalanges of the flexed
hand digits II-IV which enable the animal
to locomote via a combination of digitigrade
hands and plantigrade feet (Tuttle, 1967).
Despite the categorization as a terrestrial
quadruped, the mountain gorilla utilizes arboreal substrates for a variety of activities,
including feeding, nesting (Pitman, 1935;
Donisthorpe, 1958, Schaller, 1963;Jones and
Sabater Pi, 1971; Fossey, 1979; Tuttle and
Watts, 1985), and playing (Schaller, 1963;
Fossey, 1979; Tuttle and Watts, 1985). Earliest accounts of such activities were anecdotal but have since been confirmed by quantitative behavioral studies (Tuttle and
Watts, 1985).Not surprisingly, the frequency
with which gorillas engage in arboreal activities, including climbing, has been shown to
vary inversely with body size (Schaller, 1963;
Tuttle and Watts, 1985). This relationship
was identified initially by Schaller (1963),
who observed age- and sex-related differences in tree-climbing and arm-swinging,
and documented quantitatively more recently by Tuttle and Watts (19851, who note
that adults knuckle-walk more frequently
than either juveniles or young adults,
younger (and smaller) gorillas are more arboreal compared to the extremely terrestrial
silverbacks, and adult females utilize arboreal substrates more frequently than adult
males.
Among the various skeletal components
associated with locomotion, the scapula has
been examined extensively, perhaps because
of its evolution a s part of the shoulder complex from a weight-bearing organ in terrestrial quadrupeds to a n organ of manipulation and balance in modern humans
(Schultz, 1930; Coolidge, 1933; Ashton et al.,
1965; Oxnard, 1963,1967,1976; Preuschoft,
1973; Siege1 and Jones, 1975; Kimes et al.,
1979; Doyle et al., 1980; Shea, 1986). Variation in scapula morphology among primates
has been primarily linked to differences in
frequency of arboreal and terrestrial behaviors (Coolidge, 1933; Roberts, 1974; Oxnard,
1963, 1967). Many analyses of scapula proportions have suggested that the scapula reflects a distribution of shape change, with
extreme arboreality in the gibbons, siamangs, and orang-utans at one end of the
hominoid distribution and extreme terrestriality in gorillas and humans at the other.
Gibbons and siamangs, for example, are brachiators characterized by marked vertical
elongation of the scapula, relatively narrow
supraspinous and infraspinous fossae, and
a vertebral border obliquely sloped relative
to the scapula spine. These features have
been related to their increased ability to circumduct, to make rapid reaching movements a s they move between overhead supports, and to meet the tensile demands
placed on the shoulder joint during constant
overhead arm-swinging (Roberts, 1974).
By contrast, the gorilla, a terrestrial quadrupedal knucklewalker, bears scapulae with
very broad supraspinous and infraspinous
fossae, both of which are often further triangulated into smaller fossae presumably reflecting increased muscle mass (Roberts,
19741,and a vertebral border nearly perpendicular to the scapula spine, designed to
withstand compressive forces along the vertebral border (Roberts, 1974). Chimpanzees,
intermediate in behavior and morphology,
are described a s having narrower scapulae with less well-developed supraspinous
fossae than gorillas (Roberts, 1974); and
humans have broad, well-developed infraspinous fossae but poorly developed supraspinous fossae, reflecting the fact that
humans do not habitually elevate the upper
limb above the level ofthe shoulder (Roberts,
1974). Thus, it has been argued specifically
that primates with relatively vertically elongate, narrower scapulae and higher scapular
indices, while not necessarily converging on
the hylobatid pattern of brachiation, should
at least be better adapted to, and incorporate
with relatively greater frequency, armswinging, arm-hanging, climbing, and other
arboreal behaviors (Ashton and Oxnard,
1964; Ashton et al., 1965; Roberts, 1974;
Horn, 1975; Susman, 1980, 1984).
Locomotor behavior often changes with
SCAPULA MORPHOLOGY IN THE MOUNTAIN GORILLA
body size both between and within species.
For example, in their comparative study of
New World monkeys, Fleagle and Mittermeier (1980) demonstrated that increase in
body size among species is accompanied by a
corresponding increase in arboreal climbing
and decrease in leaping. Crompton's (1983)
study of two species of galago yielded similar
results. Doran's (1992) study of chimpanzee
locomotor behavior revealed that pygmy and
common chimpanzees undergo changes in
locomotor and positional patterns during ontogeny. Other studies have documented a
within-species relationship between differences in positional behavior and body size.
Gebo (19921, for example, found that female
Alouatta paliatta utilize smaller diameter
supports and climb more frequently than
larger males. Among the apes, Sugardjito
and van Hooff (1986) and Cant (1987)
showed that sexual dimorphism in body size
correlates with differences in positional behavior between male and female orangutans. Doran (1993) found that sexual dimorphism in body size correlates with differences in positional behavior between adult
male and female chimpanzees.
Despite evidence of a within-species correlation between body size and locomotor behavior, studies establishing a within-species
relationship among body size, locomotor behavior, and skeletal morphology in primates
are lacking. Shea (1986) demonstrated that
scapula proportions differ between subadult
and adult chimpanzees, and these morphological differences have been purported t o
correlate with age-related changes in locomotor behavior (Doran, 1992). If changes in
body size influence the relationship between
form and function, then such effects should
be most apparent in a species like Gorilla
which exhibits a wide range in body size during the life cycle. Therefore, this study investigates the effects of ontogeny and sexual
dimorphism on scapula morphology in one
subspecies of Gorilla (G.g. beringei).Specifically, this work evaluates whether sexual differences in scapula morphology are the results of ontogenetic scaling, whether scapula
form varies with age, and whether any
sex- or age-related differences in scapula
form correlate with differences in locomotor
behavior.
433
MATERIALS AND METHODDS
Samples
The scapulae and associated skeletal and
cranial material for G.g. beringei were obtained from the collections of the Musee
Royal de l'Afi-ique Centrale (Tervuren, Belgium), Musee de la Vie (Louvain-La-Neuve,
Belgium), the National Museum of Natural
History (Washington, DC), and the Comparative Museum of Zoology (Cambridge, MA).
Measurements were taken entirely from
wild-caught specimens of known locality.
For comparisons of age-related changes,
data are grouped into three age categories.
Age was estimated by use of a combined dental and cranial classification utilizing associated crania as follows: stage 1, all deciduous
teeth fully erupted, plus any combination of
the following: M' partially or fully erupted,
M2 partially or fully erupted, and C and M3
erupting-juvenile (n = 9); stage 2, full permanent dentition, basilar suture open, moderate wear-subadult (n = 11); and stage 3,
full permanent dentition, basilar suture
closed, heavy wear-adult
(n = 18). This
aging scheme has been utilized in previous
analyses (Korgman, 1931; Randall, 1943;
Ashton and Zuckerman, 1950; Shea, 1981)
and found to be reliable (Taylor, 1992).
Estimation of age of individuals of known
sex but lacking associated crania is by stepwise discriminant function analysis utilizing
partial skeletal weight (computed from the
combined weights of the skull, mandible,
paired femora, humeri, scapulae, and pelvis,
including the sacrum [Steudel, 1981]), humeral length, femoral length, iliac length,
and femoral circumference. Percent of
grouped cases classified correctly is 95.0%
for males and 100% for females.
Measurements
A total of six linear measurements was
obtained on each scapula (Schultz, 1930;
Shea, 1986; Takahashi, 1990) (Fig. 1). These
include 1) maximum scapula length, measured from the middle of the dorsal border of
the glenoid fossa to the point on the vertebral
margin where the medial end of the scapula
spine directly meets the vertebral border (AD), 2) total breadth, measured as the maximum straight line distance from the superior
434
A.B. TAYLOR
B
3. Infraspinous fossa lengthiscapula
length x 100;
4. Scapula lengtldspine length x 100;
5 . Spine lengthisupenor border length X
100; and
6. Supraspinous fossa lengtldinfraspinous fossa length x 100.
Methods of analysis
Two-way analyses of variance (ANOVA)
were carried out to test for significant sexand age-related differences in size and shape
of the scapula, as represented by linear measures of size and indices of shape. Each analysis treated sex and age a s independent variables and a measure of scapula size or shape
the dependent variable (Fig. 2). Tukey’s
E as
HSD post-hoc test was used to protect from
Fig, 1. Drawing of an adult male Gorilla gorilla be- declaring pairs of means different when they
ringei. Measurement definitions described in text. Re- could differ by chance, and, because counts
drawn from Schultz (1930).
of cases per cell were unequal, the harmonic
mean was utilized by applying the TukeyKramer adjustment. Results of these and all
border of the scapula to the inferior border of other analyses are considered statistically
the scapula (B-E), 3) spine length, measured significant at the P < 0.05 level. All statistifrom the point on the vertebral margin cal analyses were carried out utilizing SYSwhere the medial end of the scapula spine TAT (1992).
directly meets the vertebral border to the
Bivariate ordinary least squares (OLS)
most distant point on the acromion process and reduced major axis (RMA) regression
(A-C), 4) supraspinous fossa length, mea- analyses were carried out on log-transsured from the tip of the superior border to formed data to describe and compare allothe point on the vertebral margin where the metric growth trajectories between sexes.
medial end of the scapula spine and the ver- Analysis of covariance (ANCOVA) was used
tebral border meet (A-B), 5) infraspinous to test for significant differences in patterns
fossa length, measured from the tip of the of relative growth between OLS regressions
inferior border of the scapula to the point on for the sexes. The method described by
the vertebral margin where the medial end Clarke (1980) was used to test for significant
of the scapula spine and the vertebral border RMA slope differences between sexes and
meet (A-E), and 6) superior border length, Tsutakawa and Hewett’s (1977) “quick test”
defined here as the distance between the su- used to test for significant positional differperior border of the scapula and the tip of ences in RMA regression lines. Because samthe acromion process (B-C). All linear mea- ple sizes are small and there are only six
surements were recorded with a digital cali- bivariate comparisons, only differences idenpers accurate to 0.01 mm. Data were input tified by both line-fitting techniques were
directly into a portable personal computer considered statistically significant at P <
via a GagePort computer interface.
0.05.
From linear measures, six shape indices
were generated:
RESULTS
Scapula size
Tests
of
statistical
differences in scapula
1. Scapula lengthiscapula breadth X 100;
2. Supraspinous fossa lengthhcapula size by sex and age are all significant (Table
1). Post-hoc tests reveal significant differlength x 100;
435
SCAPULA MORPHOLOGY IN THE MOUNTAIN GORILLA
JUVENILE
SUBADULT
ADULT
d
?
Fig. 2. A two-by-three model depicting sex and age as the independent variables and scapula shape
as the dependent variable. Adapted from Schultz (1930).
ences between sexes for all scapula dimensions a t the subadult and adult stages. At
the juvenile stage, males and females are
characterized by scapulae of comparable
sizes (Table 2). Of note is that juvenile females are (not significantly) larger than
their male counterparts for all measures of
scapula size. This pattern is reversed in subadults, where males are characterized by
significantly larger scapulae than females of
comparable age. Thereafter, males remain
larger than females of comparable age for
all measures of scapula size. As expected,
sexual dimorphism in scapula size becomes
more extreme as body size and age increase.
Descriptive growth statistics for each linear measurement by age indicate t h a t
growth from juvenile to adult proceeds at a
fairly constant rate for all measures of scapula size, with juvenile males achieving approximately 45.0% and juvenile females approximately 60.0% of their full adult sizes
(Table 3). In all cases, growth from subadult
to adult is negligible, involving less than a
10% increase in size in all cases.
Scapula shape by sex and age
Tests of statistical differences in scapula
shape by sex and age are significant only for
age (Table 4). Specifically, shape ratios of
scapula length vs. scapula breadth, infraspinous fossa length vs. scapula length, and
scapula length vs. spine length vary significantly with age. In comparison to adults,
post-hoc tests reveal that juveniles have significantly higher index values for scapula
length vs. scapula breadth and significantly
lower values for infraspinous fossa length
vs. scapula length (Table 5). Juveniles have
comparatively shorter scapula spines compared with either subadults or adults.
Relative growth of the scapula
Statistical tests of slope and position differences reveal that, for the most part, males
and females are characterized by ontogenetic scaling. In other words, males and females share a common growth trajectory
such that males continue to grow along a
common growth vector after growth in fe-
436
A.B. TAYLOR
TABLE 1. Means (mm), standard deviations (Sol, sample sizes, and results of tests for statistical differences in six Linear
measures of scapula size for male and female Gorilla gorilla beringei'
Variable
Sex
Juvenile
Age
Subadult
Adult
Significance
by sex
Male
81.7
(21.9)
3
91.0
(9.9)
6
169.5
(16.9)
7
131.2
(10.9)
4
178.2
(10.5)
12
133.1
(6.4)
6
110.6
(30.2)
118.9
(19.7)
237.0
(26.3)
180.9
(16.6)
253.7
(19.5)
190.9
(10.7)
62.5
(18.4)
63.1
(9.5)
129.0
(13.2)
97.4
(12.7)
136.3
(14.7)
102.4
(7.1)
60.1
(16.7)
64.2
(12.6)
129.3
(17.9)
99.9
(8.7)
137.9
(8.1)
102.2
(4.7)
97.0
(26.6)
108.3
(14.0)
221.3
(24.5)
171.8
(16.3)
229.8
(18.6)
176.8
(11.0)
54.2
(11.2)
66.4
(7.3)
131.2
(18.9)
102.4
(14.0)
130.9
(13.7)
105.5
(9.2)
Scapula length
Female
**
Scapula breadth
Male
Female
Supraspinous fossa length
Male
Female
Infraspinous fossa length
Male
Female
Spine length
Male
Female
**
Superior border length
Male
Female
*
'Results are for mean differences between sexes at each age.
' P i 0.05.
**P < 0.001.
TABLE 2. Results of post-hoc tests for statistical differences in six linear measures of scapula size between .sexes
for each age group
Male vs. female
iuveniles'
Variable
Male vs. female
subadults
Male vs. female
adults
NS
NS
NS
NS
NS
NS
Length
Breadth
Supraspinous fossa length
Infraspinous fossa length
Spine length
Sunerior border leneth
INS, nonsignificant.
* P i 0.05.
TABLE 3. Descriptiue growth statistics by age and sex for six linear measures of the scapula'
Variable
Male
Scapular length
Scapular breadth
Supraspinous fossa length
Infraspinous fossa length
Spine length
Sunerior border leneth
45.8
43.7
45.9
43.6
42.2
41.4
Juvenile
Female
68.4
62.3
61.6
62.8
61.3
62.9
'Values represent percentage of growth as computed with adult as base.
Male
95.1
93.4
94.6
93.8
96.3
100.7
Subadult
Female
98.6
94.8
95.1
97.7
97.2
97.1
Adult
Male
Female
100.0
100.0
100.0
100.0
100.0
100.0
100.0
100.0
100.0
100.0
100.0
100.0
SCAPULA MORPHOLOGY IN THE MOUNTAIN GORILLA
437
TABLE 4. Means, standard deviations (SD),sample sizes, and results of tests of statistical differences in scapula shape
by age and sex in Gorilla gorilla beringei’
Variable*
Sex
Juvenile
Age
Subadult
Male
74.2
(6.10)
3
77.4
(7.9)
6
71.7
(5.0)
7
72.7
(4.6)
4
70.4
(2.8)
12
69.8
(3.5)
6
76.2
(5.5)
69.3
(6.6)
76.1
(2.2)
74.3
(8.2)
76.3
(5.0)
77.0
(5.5)
73.7
(9.7)
70.2
(7.3)
76.4
(8.2)
76.2
(2.5)
77.5
(3.9)
76.8
(1.8)
84.3
(2.0)
84.5
(8.3)
76.7
(2.6)
76.5
(4.8)
77.8
(3.6)
75.3
(1.5)
56.5
(3.8)
61.7
(5.7)
59.2
(4.4)
59.6
(5.7)
Significance
by age
Significance
by sex
*
NS
NS
NS
*
NS
**
NS
57.0
(4.0)
59.7
(3.7)
NS
NS
98.7
(8.5)
100.4
(7.9)
NS
NS
Adult
SCWSCB x 100
Female
SFWSCL x 100
Male
Female
IFWSCL x 100
Male
Female
SCWSPL x 100
Male
Female
SBWSPL x 100
Male
Female
SFMFL x 100
Male
103.9
1(00.5
(9.6)
97.5
(9.3)
(6.8)
Female
99.1
(7.8)
‘Tests for significant differences among age groups are with sexes combined.
‘SCL, scapula length; SCB, scapula breadth; SFL, supraspinous fossa length; IFL, infraspinous fossa length; SPL, spine length; SBL, superior
border length.
* P C 0.05.**P < 0.01.
NS, nonsignificant.
TABLE 5. Results of post-hoc tests for statistical differences in scapula shape by age’
Juvenile vs. subadult
Scapula length vs. scapula breadth
Infraspinous fossa length vs.
scapula length
Scapula length vs. spine length
NS
NS
*
Juvenile vs. adult
*
Subadult vs. adult
*
NS
NS
*
NS
’ NS, nonsignificant.
* P C 0.05.
males has ceased (Tables 6, 7, Fig. 3A-F).
Visual examination of bivariate plots reveals
that patterns of growth for shape comparisons between males and females are fairly
linear (Fig. 3A-F). For all bivariate comparisons save one, RMA regression analyses
yield higher slopes and lower y-intercepts
t h a n OLS regression analyses, the exception
being the slope and intercept comparison for
males of spine length vs. superior border
length. The trend is for females to scatter
below males (Fig. 3A-F). In all cases, correlation coefficients are sufficiently high so
that RMA slopes fall within the 95% confidence intervals of the OLS slopes.
Results of Clarke’s test for slope differences on RMA regressions did not always
concur with results of ANCOVA on OLS regressions (Table 7). Specifically, ANCOVA
reveals significant sex differences in slopes
of bivariate plots of scapula breadth against
scapula length and scapula length against
438
A.B. TAYLOR
TABLE 6. OLS and RMA regression statistics
RMA
OLS
Male
Female
Scapula length vs. scapula breadth
0.919
Slope
0.042
y-intercept
(0.847-1.051)
95% c1
R
0.98
Scapula length vs. supraspinous fossa length
Slope
0.944
y-intercept
0.235
(0.867-1.021)
95% CI
R
0.98
Scapula length vs. infraspinous fossa length
Slope
0.891
v-interceut
0.344
(0.771-1.011)
i 5 % CI
R
..
R
0.888
0.152
(0.840-0.936)
0.99
Supine length vs. superior border length
Slope
0.948
y-intercept
0.348
9 5 8 Cl
(0.853-1.043)
R
0.98
Supraspinous fossa length vs. infraspinous fossa length
Slope
0.927
y-intercept
0.150
95%
R
c1
(0.811-1.043)
0.96
Female
0.929
0.018
(0.849-1.016)
0.833
0.228
(0.729-0.952)
0.772
0.596
(0.611-0.913)
0.94
1.000
0.120
(0.914-1.094)
0.833
0.462
(0.691-1.004)
0.767
0.582
(0.680-0.854)
0.98
0.929
0.269
(0.796-1.083)
0.833
0.454
(0.747-0.930)
0.802
0.330
(0.658-0.946)
0.95
0.929
0.055
(0.871-0.990)
0.909
0.097
(0.766-1.079)
0.991
0.236
(0.819-1.163)
0.95
0.933
0.378
(0.853-1.021)
1.000
0.220
(0.843-1.186)
0.925
0.139
(0.774-1.076)
0.96
0.929
0.149
(0.818-1.054)
1.000
-0.010
(0.858-1.166)
0.717
0.333
(0.670-0.904)
0.97
0.96
. .~
Scapula length vs. spine length
Slope
y-intercept
95% CI
Male
TABLE 7. Results of OLS and RMA tests for slope and y-intercept differences between sexes'
RMA
OLS
Scapula length vs. scapula breadth
Scapula length vs. supraspinous fossa length
Scapula length vs. infraspinous fossa length
Scapula length vs. spine length
Spine length vs. superior border length
Supraspinous vs. infraspinous fossa length
SloDe
v-interceDt
SloDe
v-interceDt
*
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
*
NS
NS
NS
NS
*
NS
NS
*
NS
NS
NS, nonsignificant
* P < 0.05.
supraspinous fossa length, whereas Clarke's
test yields nonsignificant differences in
slopes for all six bivariate regression analyses. ANCOVA also reveals a significant difference between the sexes for the y-intercept
for the bivariate comparison of superior border length against spine length. Again, Tsutakawa and Hewett's (1977) significance
tests for position differences do not concur
with ANCOVA on this significant result but
rather yield a significant position difference
for the comparison of scapula length vs.
spine length. Since significant slope and intercept differences could not be substanti-
ated by both methods, results are interpreted as reflecting a pattern of similarity in
scapula shape between sexes.
DISCUSSION
As expected, data presented in this investigation reveal significant differences in
scapula size between males and females during ontogeny. Previous studies of common
chimpanzees (Gavan, 1953; Smith et al.,
1975; Shea, 1981) and gorillas (Randall,
1943; Shea, 1981; Leigh, 1992) reveal that
females tend to be larger than males at early
439
SCAPULA MORPHOLOGY IN THE MOUNTAIN GORILLA
2.6
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Fig. 3. A-F: Bivariate plots of linear regressions of scapula dimensions for Gorilla gorilla beringei
and 95% confidence ellipses. All variables are in base 10 logarithms. M, males: F, females. Associated
regression statistics presented in Tables 6 and 7.
2.5
440
A.B. TAYLOR
stages of growth but that males grow faster
and for longer duration than females. Patterns of scapula growth identified in this
study appear consistent with previous findings for the African apes. Significant differences between subadults in all dimensions of
the scapula suggest that male G.g. beringei
achieve larger adult body size by growing at
a faster rate than females (Table 2) (Gould,
1977; Shea, 1983, 1988; Ravosa et al., 1993;
Ravosa and Ross, 1994). This pattern is evident, for example, in the increase in scapula
length. The average subadult male scapula
is 169.5 mm in length, which is approximately 95% of its average adult length of
178.2 mm. The average subadult female
scapula is 131.2 mm in length, approximately 99% of its average adult length of
133.1 mm. Therefore, males grow a t a faster
rate than females because they undergo a
greater increase in length compared to juvenile females and as adults they have longer
scapulae than females. The marked increase
in differences in scapula size from subadult
to adult suggests that males also attain
larger adult body size by growing for longer
duration; that is, males continue to grow
after growth in females is complete.
Although not statistically significant, juvenile females achieve a greater percentage
of their adult scapula size compared to juvenile males. Interestingly, similar data for
lowland gorillas for which data on infants
and larger sample sizes were available reveal nonsignificant differences between infant males and females and that males are
consistently larger than females throughout
growth (Taylor, 1992, in preparation). One
explanation for these subspecies differences,
and for the discrepancy between previous
findings of growth for the African apes and
results for lowland gorillas, is that the aging
scheme utilized in this investigation for
identifying juveniles encompasses too many
distinct growth stages. As such, the early
growth spurt typical of females would be obscured. However, since the aging criteria
were the same for both subspecies, this interpretation seems unsatisfactory. Rather, such
findings are either suggestive of true differences in patterns of growth between subspecies, or the results of small, biased sample
sizes for juvenile mountain gorillas. Larger
sample sizes and data on infants for the
mountain gorillas will undoubtedly clarify
this issue.
Age-related differences in scapula form
One of the original premises of this investigation was that changes in body size ought
to affect the relationship between form and
function, meaning that in order for animals
of differing size to accomplishthe same kinds
of tasks, changes in form must accompany
an increase or decrease in body size. It was
further argued that such changes should be
more dramatic in species characterized by
extreme ranges in body size-not simply between sexually dimorphic individuals, but
among individuals of varying size within a
single ontogeny.
Data from this investigation reveal three
significant age-related shape differences involving ratios of scapula length vs. scapula
breadth, infraspinous fossa length vs. scapula length, and scapula length vs. spine
length (Table 4). All three shape ratios differ
significantly between juveniles and adults,
and the shape ratio of scapula length vs.
spine length differs between juveniles and
subadults as well. Larger sample sizes and
data on infants would likely increase the
number of significant age-related differences, as was the case for similar data on
lowland gorillas (Taylor, 1992, in preparation).
Mean scapula length for juveniles is approximately 82.0 mm and mean scapula
breadth approximately 111.0 mm (Table 1).
These lengths are essentially doubled in subadults, where mean length is 170.0 mm (an
increase of about 107.0%)and mean breadth
237.0 mm (an increase of approximately
114.0%).These two values have more than
doubled, however, since increase in scapula
length and breadth by exactly 100% would
result in values of 164.0 mm and 222.0 mm,
respectively. Mean length exceeds an increase of 100% by 6.0 mm, mean breadth by
15.0 mm. In other words, as size increases
scapula breadth not only remains longer
than scapula length, but its rate of increase
is greater relative to that of scapula length,
resulting in subadults with absolutely and
relatively broader scapulae compared to juveniles. It is important to note that a rela-
SCAPULA MORPHOLOGY IN THE MOUNTAIN GORILLA
tively broader scapula is more vertically
elongated (that is, longer and narrower perpendicular to the scapula spine). The longer
infraspinous fossa length relative to scapula
length in juveniles compared to adults reflects this vertical elongation (Table 3).
At larger body sizes, scapula breadth continues to grow a t a faster rate than scapula
length, resulting in the well-established pattern for gorillas of scapulae with markedly
broad fossae, in particular with relatively
broader supraspinous fossae compared to
any other primate (Roberts, 1974). Rate of
increase along both dimensions slows considerably a s gorillas approach full adult size.
Adult male scapulae are only about 5%
longer and 7% broader than subadults. The
pattern is the same for females, except percentage of growth from subadult to adult is
less than for males, confirming that females
grow for shorter duration (Table 3).
Variation in length vs. breadth index, referred to by Schultz (1930) as the “scapula
index,” has been linked to various functional
differences in behavior among primates. I t
has been well established that high index
values for the ratio of scapula length vs.
scapula breadth are characteristic of proportionately narrow scapulae, as are low indices
for infraspinous fossa length vs. scapula
length. Ashton and Oxnard (1963) have suggested that narrow and elongated scapulae,
such as are characteristic of the gibbon and
siamang, provide increased mechanical advantage to scapula stabilizers and rotators,
such as the serratus anterior and trapezius
muscles. They argue the comparatively high
index of the gibbons affords these animals
greater range of motion and increased joint
stability, mechanical advantages necessary
for withstanding tensile forces involved in
grasping overhead supports during mid-air
propulsion (Ashton and Oxnard, 1963). Roberts (1974) has echoed this claim, suggesting
that the gibbon’s narrow scapula is designed
to provide increased circumduction and joint
stabilization to the shoulder.
More recently, it has been suggested that
the long, narrow scapula of the chimpanzee
is related to a n increase in ability to abduct
and upwardly rotate the humerus during
unimanual arm-hanging, thereby achieving
a relatively close approximation of the gleno-
44 1
humeral joint to the spinal column and reducing the mechanical stresses associated
with arm-hanging behavior (Hunt, 1991).
These hypotheses focus on the mechanical
advantages afforded the serratus anterior
and trapezius muscles, and the concomitant
reduction in mechanical stresses, and suggest that arm-hanging and brachiation are
kinematically similar behaviors requiring
similar bony and muscular adaptations.
Values €or the scapula index in mountain
gorillas range from about 77.0 for juveniles
to 70.0 for adults (Table 4). Of interest are
data on lowland gorillas for which individuals of dental stage 1(infants)were available
(Taylor, in preparation), revealing a higher
scapula index for infants compared to juveniles (82.0 for infants as compared to 74.0
for juveniles) and increasing the range for
this index by about 4%. A reasonable inference is that data on G.g. beringei infants
would similarly increase the range for mountain gorillas and result in a higher frequency
of significant age-related differences.
One could predict that a high scapula index would be associated with behaviors such
as suspensory locomotion, arm-hanging,
arm-swinging, and, perhaps, vertical climbing, whereas a relatively low index would be
associated with more terrestrial quadrupedal behaviors. Data from this study indicate
that juveniles are characterized by relatively
higher scapula indices than either subadults
or adults, suggesting that younger gorillas
should be incorporating a greater component
of arm-hanging behaviors than at any other
stage of growth-a prediction based not only
on the assumption that small body size facilitates activities which are prohibitive a t
larger body sizes but that scapula form in
younger individuals is better suited to such
behaviors. In fact, these predictions are
borne out by behavioral data which indicate
that frequency of arboreal activity is higher
in younger, smaller individuals than in older,
larger ones (Schaller, 1963; Goodall, 1977;
Tuttle and Watts, 1985).
In this study, data reveal that subadults
and adults have significantly longer scapula
spines compared to scapula lengths than juveniles (Tables 1,5). Schultz (1930) has suggested the length vs. spine length index reflects the relative extent to which the
442
A.B. TAYLOR
acromion process extends beyond the level
of the glenoid fossa, postulating that a relatively longer spine and acromion process
provide increased protection of the shoulder
joint. Roberts (1974) hypothesized that the
acromion functions in a bridge-like manner
to provide structural support and increased
leverage for the deltoid muscle. More recently, i t has been suggested (Takahashi,
1990) that a well-developed scapula spine
is logically a function of increased muscle
attachment of the trapezius and deltoid muscles, thus a t least partially echoing Roberts’s
earlier claim. Takahashi’s results led her to
conclude that a well-developed spine in Hylobates functions to increase the mechanical
advantage of these muscles in elevating the
humerus during arm-swinging, although
she admits that such muscles are equally
important in vertical climbing as well.
Therefore, the presence of a well-developed scapula spine in the mountain gorilla
may serve a dual advantage. First, a welldeveloped scapula spine provides a n increased mechanical advantage in elevating
the humerus during arm-hanging activities,
especially in younger individuals with lessdeveloped associated muscles, articulations,
and ligaments to reinforce the glenohumeral
joint. Second, the mechanical advantage of
the trapezius and deltoid muscles is enhanced, particularly in larger, heavier individuals who not only vertically climb, but
who frequently use their upper limbs in a n
abducted position during feeding (Roberts,
1974; Tuttle and Watts, 1985). Tuttle and
Watts (1985) found a n inverse relationship
between forelimb length and frequency of
humeral protraction above the shoulder joint
during feeding bouts in the mountain gorilla.
These data support the hypothesis that increased leverage of muscles associated with
humeral abduction is particularly advantageous in larger individuals.
Larson and Stern (1986) have demonstrated that electrical potentials of the supraspinatus and deltoid muscles in chimpanzees are highest during the initial phases
of humeral elevation, during which these
muscles are active in resisting the tendency
of the deltoid muscle to displace the humerus
superiorly. Recent studies in chimpanzee positional behavior (Hunt, 1991,1992) indicate
that chimpanzees require a fully abducted
humerus during arm-hanging and large
muscles for arm-raising, such as teres minor,
cranial trapezius, anterior deltoid, and clavicular portion of pectoralis major (Hunt,
1991). These data also strengthen the suggestion that a relatively long scapula spine
is mechanically advantageous in humeral elevation during climbing and hanging activities.
Sex differences in scapula form
The pervasive pattern for mountain gorillas is one of similarity in scapula form between sexes. Comparisons of male and female regressions suggest that differences in
scapula proportions between adults result
from extension of common patterns of relative growth (Tables 4, 7; Fig. 3A-F). With
the exception of the two shape indices involving the length of the spine (Fig. 3D-E), the
trend is for males and females to overlap at
smaller sizes and diverge through time, with
females shifting below males and males continuing to grow to larger terminal sizes.
The effects of sexual dimorphism on locomotor (Fleagle and Mittermeier, 1980;
Doran, 1993),positional (Cant, 1987; Doran,
1993), and feeding behaviors (Wrangham
and Smuts, 1980; Galdikas and Teleki, 1981;
Cant, 1987) have been well documented. By
contrast, few studies have correlated behavioral differences between sexes with genderspecific morphologies. This study suggests
that, despite differences in locomotor behavior between sexes, there is little evidence to
suggest that males and females have evolved
unique morphological adaptations to different ecological niches. Results of this investigation also raise the issue of whether frequency or kinematics (Prost, 1965, 1967) is
the relevant variable in correlating morphology with behavior. This issue is particularly
germane to studies attempting to identify
gender-specific morphological patterns,
since the “average biomechanical situation”
(Oxnard, 1979) will likely be more similar
between sexes than between species, potentially obscuring subtle differences. Although
tempting to attribute the absence of significant proportion differences between sexes to
small sample sizes, a similar analysis of sexual differences for lowland gorillas for which
SCAPULA MORPHOLOGY IN THE MOUNTAlN GORILLA
sample sizes were notably larger yielded results similar to those found for the mountain
gorilla (Taylor, 1992, in preparation).
SUMMARY AND CONCLUSIONS
The purpose of this investigation was to
assess the effects of ontogeny and sexual dimorphism on scapula form in the mountain
gorilla and to correlate any differences in
scapula morphology with variability in locomotor behavior. Data reveal significant agerelated variability in scapula form. However,
sexual differences in shape of the scapula
can be explained by ontogenetic scaling of
scapula proportions. Ontogenetic differences
in scapula form in gorillas are suggestive of
locomotor differences relating to frequency
of arboreal vs. terrestrial behaviors. Thus,
younger and more actively arboreal gorillas
appear to fit a morphological pattern which
more closely approximates the hylobatid
pattern of vertically elongated and mediolaterally compressed scapulae.
Previous comparisons of scapula form in
chimpanzees have revealed significant proportion differences between adult common
and pygmy chimpanzees which reflect form
differences between subadult and adult common chimpanzees (Shea, 1986). Given the
proportion differences among mountain gorillas of varying agelsize, it would be worthwhile to determine if differences in scapula
form between subspecies reflect the specific
proportion differences documented among
age groups. Such data would enable us to
distinguish between genetic-based differences in scapula form and those related to
remodelling during growth.
Behavioral data on the lowland gorilla are
emerging from the field (Remis, 1994,1995).
In addition, recent genetic data strongly support a greater degree of separation between
the two subspecies of gorilla than had been
previously accepted (Ruvolo e t al., 1991; Ruvolo, 1994). These data suggest the need for
a more comprehensive investigation of variability in locomotor morphology, including
the scapula, both within and between species. Such data would enhance our understanding of patterns of variability and lead
to a fuller appreciation of the functional
443
implications of morphological variability
among the African apes.
ACKNOWLEDGMENTS
I thank M.I. Siegel, B.T. Shea, and M.D.
Rose for helpful comments and suggestions.
This manuscript benefited greatly from the
comments and criticisms of two anonymous
reviewers. I am grateful for the support and
assistance of Dr. W. Van Neer, Dr. R.W. Thorington, Ms. M. Rutzmoser, and the staffs of
the Musee Royale de l’Afrique Centrale, the
National Museum of Natural History, and
the Museum of Comparative Zoology. I am
particularly indebted to Bernard and MariePaul Latteur (MusBe de la Vie) for their gracious hospitality during my stay in Belgium.
This research was supported by the National
Science Foundation (BNS 90-16522), Wenner-Gren Foundation (Gr. 53231, Sigma Xi
Grants-in-Aid of Research, and a Mellon
Predoctoral Fellowship award.
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morphology, beringei, effect, mountain, dimorphic, scapular, sexual, gorillas, ontogeny
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