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Craniodental allometry and heterochrony in two howler monkeys Alouatta seniculus and A. palliata

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American Journal of Primatology 33:277-299 (1994)
Craniodental Allometry and Heterochrony in Two Howler
Monkeys: Alouatta seniculus and A. palliata
MATTHEW J. RAVOSA’,” AND CALLUM F. ROSS3
‘Department of Cell and Moleculur Biology, Northwestern University Medical School and
’Department of Zoology, Division of Mammals, Field Museum of Natural History, Chicago,
Illinois, and 3Department of Anatomy and Human Biology, University of the Witwatersrand
Medical School, Johannesburg, Republic of South Africa
Cranial dimensions were collected from growth series for two sexually
dimorphic congeners: Alouatta seniculus, the red howler monkey, and Alouatta palliata, the mantled howler monkey. In both A. seniculus and A.
palliata, ontogenetic series for males and females were compared to evaluate if sexual dimorphism in skull form results from the differential extension of common patterns of relative growth. Subsequently, growth series
for both species were compared to investigate whether morphological differences between species also result from the ontogenetic scaling of cranial
proportions.
Analyses indicate that cranial proportions for both sexes of Alouatta
palliata are ontogenetically scaled. In mantled howlers, males apparently
reach larger terminal size by growing for a longer duration and, to a lesser
extent, a t a faster rate than females. Data for both sexes of Alouatta
seniculus indicate that cranial proportions are also ontogenetically scaled.
In particular, male red howlers apparently reach larger adult size by growing at a faster rate and, perhaps, to a n equivalent or longer duration than
females. The Alouatta seniculus data underscore apparent differences in
the rate and timing components of sex dimorphism, possibly due t o sexual
differences among dental eruption patterns, cranial development, somatic
growth, and socioecological factors. Results for both species indicate that
intrasexual selection for size differentiation has a minimal effect on brain
size and postcanine tooth size dimorphism. Lastly, comparisons of allometric trajectories for both species further demonstrate a strong pattern of
ontogenetic scaling of cranial proportions. 0 1994 Wiley-Liss, Inc.
Key words: allometry/scaling, skull form, ontogeny, heterochrony, red
howlers, mantled howlers
INTRODUCTION
Among living platyrrhine primates, howler monkeys are among the largest
and most sexually dimorphic taxa [Schultz, 19601. Allometric and heterochronic
analyses offer a unique perspective on sexual dimorphism, in large part because
Received for publication July 8, 1992; revision accepted January 18, 1994.
Address reprint requests to Dr. Matthew J. Ravosa, Department of Cell and Molecular Biology, Northwestern University Medical School, 303 East Chicago Avenue, Chicago, IL 60611-3008.
0 1994 Wiley-Liss, Inc.
278 I Ravosa and Ross
such approaches address the developmental or ontogenetic processes underlying
patterns of size differentiation within and between species. In this regard, recent
work on a variety of primates demonstrates that the vast majority of sexual differences in adult cranial morphology result from the differential extension of
shared patterns of relative growth [Cheverud & Richtsmeier, 1986; Cochard, 1985;
Cole, 1990; Corner & Richtsmeier, 1991, 1992, 1993; Hays, 1990; Leigh & Cheverud, 1991; Masterson & Leutenegger, 1992; Ravosa, 1991a,b, 1992; Richtsmeier &
Cheverud, 1989; Richtsmeier et al., 1993; Shea, 1985a, 1986, 19881. Sexually dimorphic taxa characterized by this pattern of differentiation are typically referred
to as ontogenetically scaled lsensu Gould, 1975al.
These allometric analyses are also well suited to determining if there are
specific sexual differences in skull form which are not related to intrasexual selection for size differentiation. Ostensibly, they allow us to apply an ontogenetic
criterion of subtraction to secondary sexual structures and functional aspects of
skull form. One region of the skull where male howler monkeys might be expected
to exhibit relatively larger structures is the hyoid and functionally associated
features of the the mandible such as the depth of the ascending ramus and breadth
of the gonial region [Cole, 1990; Crockett & Eisenberg, 1986; Hershkovitz, 1949;
Schultz, 1960; Thorington et al., 19791. In this case, males might be predicted t o
have a relatively broader bigonial region and deeper ascending ramus in order to
accommodate a relatively larger hyoid apparatus.
In a sexually dimorphic species, where males and females show a pervasive
pattern of ontogenetic scaling and males are peramorphic via hypermorphosis,
there are two ways for males to reach a larger terminal sizes relative to the
ancestral or primitive condition of females [Shea 1983a, 1986,19881.First, one can
examine rate of growth-in-time to determine if males grow faster via rate hypermorphosis. In this case, during ontogeny males develop progressively larger craniofacial dimensions than females of the same age but mature at the same chronological age. Second, one can examine time of growth shut off to distinguish if
males grow for a longer duration via time hypermorphosis. That is, at the same
non-adult age as females, males have similarly sized craniofacial dimensions but
mature a t a later chronological age. This disparity in the amount of time it takes
the sexes to reach adulthood is termed bimaturism [Wiley, 19741. Obviously, both
processes can affect the evolution of sexual dimorphism if developmental modifications occur early in ontogeny and are particularly accentuated between nonadults and adults of each sex.
There are several caveats inherent to this type of analysis. First, this scenario
assumes that the female ontogenetic trajectory and adult body size represent the
ancestral pattern, which is often, but not always, the case; sometimes, the female
pattern may be derived [Shea, 19861. Second, this scenario does not necessarily
assume that both sexes have the same neonatal size, just that absolute differences
in neonatal body size between sexes will be much less than adult differences in
overall size [Ravosa, 1992; Ravosa et al., 19931. Moreover, as used in this context,
faster (rate) and longer (time) characterizations refer to growth-in-time, not different coefficients (regression slopes) of relative or allometric growth.
These two patterns of sexual differentiation have been linked to different
reproductive strategies [Jarman, 1983; Leigh, 1992; Ralls, 1977; Shea, 1986;
Wiley, 19741 which are relevant to an analysis of the ontogeny of sexual dimorphism in howler monkeys. According to several sources [e.g., Crockett & Eisenberg, 1986; Thorington et al., 19791, males of Alouatta palliata, the mantled
howler, have genitalia that mimic those of females until puberty, whereas males of
Alouatta seniculus, the red howler, have precocious scrota1development, much like
Cranial Growth and Scaling in Howler Monkeys I 279
juveniles of other howler species. Thorington et al. 119791 argue that the early
onset of male-female differences in red howlers serves as a status symbol within
an age-graded hierarchy, whereas the later onset of male-female differences in
mantled howlers serves to delay male-male competition for reproductive access to
females. Presumably, similar intraspecific patterns of male-female differentiation
via ontogenetic scaling might be reflected in the growth of the skull.
Based on previous analyses of skull form, there are several morphological
consequences of sexual differentiation via ontogenetic scaling. If the sexes demonstrate a consistent pattern of ontogenetic scaling of cranial dimensions, brain
size may demonstrate a dissociation of shared patterns of relative growth. This is
because intrasexual selection for size differentiation between the sexes apparently
targets primarily postnatal systemic growth. Therefore, in comparisons between
ontogenetically-scaled taxa, sexual differences in brain size, a structure that develops mostly during the prenatal growth period, are predicted to be minimal
compared to differences in other facial or somatic dimensions that develop and
enlarge mainly postnatally [Gould, 1975a; Lande, 1979; Ravosa, 1991a, 1992;
Riska & Atchley, 1985; Shea, 1983b, 1988; Shea et al., 19871.
Dental scaling patterns also mirror those for brain size across and within
ontogenetically-scaled taxa. For example, it has been demonstrated that sexual
differences in postcanine tooth size are predicted to be minimal as compared to
dimorphism in other regions of the facial skull. This is thought to occur because
genetic and epigenetic controls on dental morphogenesis operate more independent
of systemic effects on cranial growth in particular and somatic growth in general
[Cochard, 1985,1987; Gould, 197%; Ravosa, 1991a, 1992; Shea, 1988; Shea et al.,
1990; Shea & Gomez, 19881.Therefore, in an ontogenetically-scaled series of males
and females, regardless of whether selection has acted to increase or decrease
overall size intraspecifically, postcanine tooth size is expected to scale with negative allometry across adults such that larger-bodied males should have relatively
smaller teeth than smaller-bodied females le.g., Cochard, 1985, 19871. It is important t o stress that predictions of negative or positive allometry of postcanine tooth
dimensions differ from empirical data for interspecific series of anthropoid primates [Gingerich et al., 1982; Kay, 1975, 19781 and other mammals [Creighton,
1980; Fortelius, 1985; Legendre & Roth, 19881, which indicate that postcanine
tooth size generally scales with isometry vs. body mass. In a broader sense, ontogenetically-scaled taxa will show greater differentiation in aspects of skull size
relative to postcanine tooth size (and brain size) as a result of intrasexual selection
primarily on postnatal facial growth.
In this study, allometric comparisons are made within and between ontogenetic series for two howler monkeys: Alouatta seniculus and Alouatta palliata. In
both taxa, adult males outweigh adult females considerably. A . seniculus males
weigh 7,200 grams and females weigh 5,600 grams, whereas in A. palliata, on
average, males weigh 7,150 grams and females weigh 5,350 grams [Ford & Davis,
19921. This study evaluates if sexual dimorphism in howler monkey skull form
evolved via ontogenetic scaling; the effects of ontogenetic scaling on patterns of
facial, dental, and neural dimorphism; whether cranial sexual dimorphism develops via differences in growth rate andior the duration of growth; and, given a
pervasive pattern of ontogenetic scaling among the sexes, if both species share
similar patterns of relative growth. Comparisons in these two howler monkeys will
highlight the developmental bases of primate sexual dimorphism in general and,
more specifically, augment a growing number of studies regarding growth and
dimorphism in New World monkeys [i.e., Corner & Richtsmeier, 1991, 1992,1993;
Cole, 1990; Leigh, 1992; Schultz, 19601.
280 I Ravosa and Ross
MATERIALS AND METHODS
Samples
The two ontogenetic samples consist of 85 crania of the red howler monkey,
Alouatta seniculus (20 adults and 65 juveniles), and 100 crania of the mantled
howler monkey, Alouatta palliatu (2C adults and 80 juveniles). For comparisons of
craniofacial development between the sexes, the data are grouped into five dental
age classes: 1, only deciduous dentition erupted; 2, permanent 11, 12, and M1
erupted; 3, permanent M2 erupted; 4,permanent P2, P3 and P4 erupted; and 5,
permanent C and M3 erupted (adult). In A . seniculus, there are a minimum of
eight males and four females for each non-adult dental age class, whereas in A .
palliata, there are a minimum of four males and ten females for each non-adult
dental age class. Adults in both species are represented by ten males and ten
females.
Measurements
Craniometric data were recorded with digital calipers accurate to 0.1 mm. A
total of 33 linear and two volumetric measures were taken on each specimen (see
Appendix). Dimensions from bilateral structures such as orbit height were taken
on the right side of the skull; postcanine toothrow length was obtained only for
adults. Neurocranial and orbital volume were determined by filling the braincase
and orbital cavity with barley until a level surface was reached at the foramen
magnum and orbital aperture, respectively, and then pouring the barley into a
cylinder graduated in milliliters. Owing to the lack of associated field data, adult
body weight means for the sexes of both species were taken from Ford and Davis
[19921.
Statistical Analyses
Within each of the two ontogenetic series, least-squares bivariate regression
(P < 0.05) was applied to log-transformed craniometric data t o describe allometric
growth trajectories. In bivariate analyses where the correlation coefficient was
below a value of 0.90, reduced major-axis regression equations were also calculated. As is common for most ontogenetic studies of primate cranial allometry,
basicranial length was used as the independent variable in all bivariate comparisons. In comparisons of linear dimensions vs. basicranial length, isometry equals
a slope of 1.00; however, for volumetric measures, isometry equals a slope of 3.00.
For regression analyses in both species, the data were averaged by dental age and
sex, in part so as to reduce the effects of disproportionately large numbers of
individuals of a particular dental age on the slope o f the regression line. For
instance, since adults lie at one end of the size range, greater numbers of adult
cases might bias the calculation of the regression line and thereby potentially
result in a lower regression coefficient. However, averaging the data by dental age
may mask more complex allometric growth patterns. In this study, visual inspections of individual plots suggest that this is not a significant problem with the
howler data (e.g., Figs. 1,2,5-7, 9-11, but see Fig. 3).
Analysis of covariance (ANCOVA,P < 0.05) was used to test for differences in
patterns of relative growth between regression lines derived for males and females,
and for regression lines derived for each howler monkey species (sexes pooled).
Such analyses were supplemented by visual inspections of the data. For intra- and
inter-specific comparisons, the null hypothesis is that the sexes and species are
ontogenetically scaled. However, ontogenetic scaling might not be expected in the
gonial region of the mandible due to the enlarged hyoid apparatus of males [Cole,
19901.
Cranial Growth and Scaling in Howler Monkeys I 281
T tests (P < 0.05) were used to test for sexual differences in the size of cranial
measures at common dental ages. Principal components analysis (PCA) using a
covariance matrix [Shea, 1985b, 19921 was used to describe multivariate patterns
of cranial growth and sexual differentiation; PCAs were performed on data averaged by dental age and sex. Owing to missing data for females at dental age 1in
Alouatta seniculus, browridge height, neurocranial volume, and orbital volume
were excluded from all principal components analyses. Given a pervasive pattern
of ontogenetic scaling for the sexes (or species), significant differences between
male and female raw measures andor PCA scores at common non-adult dental
ages would indicate that sexual dimorphism develops via rate hypermorphosis.
This assumes that dental ages in males and females correspond to similar chronological ages [e.g., Chase & Cooper, 1969; Johnston et al., 1970; Long & Cooper,
19681, although this is not always the case [e.g., Conroy & Mahoney, 1991; Fleagle
& Schaffler, 1982; Garn & Lewis, 1957; Hurme & van Wagenen, 19611.In addition,
this characterizes dental ages as representing equivalent time periods. Morphological differences noted only at adulthood would indicate that dimorphism develops via time hypermorphosis. If size differences are noted between the sexes during
the early stages of ontogeny and are particularly marked between adults, then this
would suggest that sexual dimorphism evolved via both heterochronic processes
[Ravosa, 1991a, 1992; Shea, 1983a, 1986, 19881.
Within each species, sexual dimorphism ratios were calculated for the adult
means of each cranial measure (i.e., adult male meadadult female mean), with a
value of 1.00 indicating that the sexes are monomorphic for that measure. Subsequently, the dimorphism ratios were ranked in descending order to investigate the
effect of sexual differentiation on relative brain size and postcanine tooth size.
RESULTS
Red Howler Monkey Comparisons
In Alouatta seniculus, all bivariate regressions vs. basicranial length are
highly correlated (Table I). Regression coefficients range from strong negative
allometry for neurocranial volume and bitemporal breadth to strong positive allometry for ramus height and mandibular corpus height. Between-sex comparisons
(ANCOVAs)of allometric growth trajectories for A . seniculus are not significant in
32 of 33 cases, which indicates a very pervasive pattern of ontogenetic scaling of
cranial proportions (Table I; Figs. 1-3). Thus, in red howlers, morphological differences between adults of each sex are due primarily to the differential extension
of common patterns of relative growth.
7'-tests at dental ages 1 and 2 between cranial measures for male and female
A. seniculus are not significantly different (Table 11).However, at dental age 1
most male measures tend to be larger than those for females, though none of these
differences are statistically significant (Table 111). Only at dental age 2 is this
pattern reversed, such that female means exceed the means for males; a plot of
PCA Factor I scores versus dental age shows a similar multivariate pattern of
sexual differentiation (Fig. 4).While this might reflect the earlier onset of an
adolescent growth spurt in females, larger females a t a common dental age could
reflect a fast rate of male dental eruption coupled with a stable (or decreasing)
male growth rate. Alternatively, a slow rate of female dental eruption coupled with
a stable (or increasing) growth rate would also explain this pattern.
By dental age 3,7 of 36 t tests are significant, and most male red howler means
for cranial measures exceed the means for female measures; this pattern continues
282 I Ravosa and Ross
TABLE I. Bivariate Regression Analyses (Sexes Pooled)*
Y-Int
Slope
95% CI
r
Alouatta seniculus
Browridge height (NS)"
Browridge height
Postorbital bar width (NS)
Zygomatic arch height (NS)
Zygomatic arch width (NS)
Zygomatic arch width
Symphysis height (NS)
Symphysis width (NS)
Symphysis width
Outer biorbital breadthb
Inner biorbital breadth [NS)
Interorbital breadth (NS)
Orbit height (NS)
Orbit width (NS)
Upper palate breadth (NS)
Bicanine breadth (NS)
Palate length (NS)
Lower skull length (NS)
Upper face height (NS)
Bizygomatic breadth (NS)
Bigonial breadth (NS)
Bieondylar breadth (NS)
Bicoronoid breadth (NS)
Ramus height (NS)
Temporal fossa length (NS)
Bitemporal breadth (NS)
Bitemporal breadth
Bipterygoid breadth (NS)
P3 bite point length (NS)
M2 bite point length (NS)
M2 corpus height (NS)
M2 corpus width (NS)
M2 corpus width
Masseter lever arm length (NS)
Temporalis lever arm length (NS)
Medial pterygoid lever arm length (NS)
Orbital volume (NS)
Neurocranial volume (NS)
Neurocranial volume
-5.211
-14.460
-7.023
-6.366
-5.378
-15.291
-3.232
-3.802
- 13.051
0.961
0.661
-4.861
0.979
1.020
0.366
-3.350
1.238
-2.999
-4.584
- 1.177
-4.129
- 1.474
- 1.094
-9.917
-3.716
4.196
1.767
-1.189
-3.467
6.606
8.070
- 0.486
-6.002
-4.758
-4.929
-3.631
- 10.187
1.249
-2.928
1.276
1.462
1.650
1.641
1.283
1.567
1.372
1.292
1.462
0.824
0.857
1.465
0.682
0.666
0.863
1.386
0.763
1.522
1.644
1.193
1.570
1.216
1.140
2.529
1.439
0.292
0.384
1.007
1.555
2.007
2.093
0.744
0.872
1.704
1.658
1.483
1.878
0.428
0.658
10.252
0.873
10.167
"0.230
10.318
0.961
0.930
0.819
20.167
?0.241
0.946
0.884
50.029
k0.044
t0.085
50.051
?0.053
+0.109
50.097
20.029
20.084
20.172
50.110
20.143
~0.125
k0.074
k0.334
20.122
50.088
0.995
0.990
0.987
0.979
0.975
0.941
0.981
0.970
0.988
0.959
0.968
0.968
0.960
0.984
0.937
0.973
0.760
20.113
20.129
k0.183
20.287
50.161
0.953
0.974
0.968
0.933
0.853
20.109
t0.141
k0.127
20.233
50.189
0.984
0.972
0.972
0.950
0.651
Alouatta palliata
Browridge height (NS)
Browridge height
Postorbital bar width (NS)
Postorbital bar width
Zygomatic arch height (NS)
Zygomatic arch height
Zygomatic arch width (NS)
Zygomatic arch width
Symphysis height (NS)
Symphysis widthb
-16.013
-18.857
-6.326
-9.099
-2.047
-3.612
-3.755
-5.113
-2.229
-2.180
2.972
20.639
0.869
10.362
0.774
20.219
0.799
10.214
0.831
50.100
0.962
0.902
vs. Basicranial length
~
~
3.420
1.531
1.978
1.008
1.262
1.064
1.280
1.222
1.063
C0.147
(continued)
Cranial Growth and Scaling in Howler Monkeys / 283
TABLE I. Bivariate Regression Analyses (Sexes Pooled)* (Continued)
vs Basicranial length
Y-Int
Slope
95% CI
r
Outer biorbital breadth (NS)
Inner biorbital breadth (NS)
Interorbital breadthb
Interorbital breadth
Orbit heightb
Orbit width (NS)
Upper palate breadth (NS)
Bicanine breadth (NS)
Palate length (NS)
Lower skull length (NS)
Upper face height (NS)
Bizygomatic breadth (NS)
Bigonial breadth (NS)
Bigonial breadth
Bicondylar breadth (NS)
Bicoronoid breadth (NS)
Ramus height (NS)
Temporal fossa length (NS)
Bitemporal breadth (NS)
Bitemporal breadth
Bipterygoid breadth (NS)
P3 bite point length (NS)
M2 bite point length (NS)
M2 bite point length
M2 corpus height (NS)
M2 corpus width (NS)
M2 corpus width
Masseter lever arm length (NS)
Temporalis lever arm length (NS)
Medial pterygoid lever arm lengthb
Orbital volume (NS)
Neurocranial volume (NS)
Neurocranial volume
1.454
1.459
- 1.289
-2.042
-0.410
1.209
0.151
-1.353
1.238
-0.045
- 1.550
-0.309
0.046
-0.939
1.855
1.761
-6.676
-3.897
4.139
3.670
-0.528
0.232
0.794
-0.103
-4.587
0.979
0.314
--0.457
-0.647
1.266
-8.735
1.065
0.739
0.745
0.733
0.901
1.022
0.907
0.644
0.895
1.072
0.763
1.047
1.159
1.068
0.904
1.061
0.694
0.690
2.024
1.469
0.301
0.376
0.886
0.967
0.842
0.985
1.544
0.529
0.636
1.026
0.983
0.708
1.654
0.454
0.506
t0.089
20.078
t0.139
0.924
0.938
0.882
50.123
20.129
k0.128
10.029
20.102
50.117
50.101
k0.168
0.905
0.945
0.904
0.924
0.970
0.947
0.944
0.950
0.852
?0.079
20.092
20.186
+0.130
10.068
0.935
0.914
0.953
0.956
0.800
50.119
50.099
50.154
0.906
0.947
0.855
10.153
co.102
0.946
0.832
t0.099
50.120
t0.103
20.159
t0.067
0.953
0.927
0.901
0.953
0.898
5 0.064
*In bivariate comparisons with r < 0.90, least-sqaures regression analyses are indicated on the first line, while
reduced major-axis regression analyses are indicated second.
"NS, no significant differences between regression lines for the sexes, P > 0.05.
bSignificant Y-intercept differences between the sexes' growth trajectories with the male line transposed above
that for females, ANCOVA, P < 0.05.
through adulthood (see also Fig. 4).This pattern is slightly accentuated at dental
age 4,where 8 of 36 comparisons reveal significantly different mean values between the sexes, with males being larger. At dental age 5, t tests between cranial
measures for adult males and females are significant in 32 of 36 comparisons;
again, males are consistently larger in size. In the other four cases, male measures
are larger, but not significantly different than those for females.
In A. seniculus, ranked dimorphism ratios of 36 cranial dimensions indicate
that neurocranial volume (32nd of 36) and postcanine toothrow length (33rd of 36)
have two of the lowest values (Table IV). This corroborates predictions regarding
the dissociation of brain size and postcanine tooth size from selection for body size
differences between the sexes. In contrast, body weight has one of the higher
dimorphism ratios (8th of 36). Bigonial breadth (2nd of 36) and ramus height (3rd
of 36) likewise have very high values, which might be expected, based on the high
284 I Ravosa and Ross
Fig. 1. Alouatta senzculus. A plot of In lower skull length vs. In basicranial length. Note that both sexes of red
howlers lie along the same ontogenetic trajectory, with differences between adults due to the differential extension of shared growth allometries. This typifies all but one bivariate comparison for this species. In of 1*10-'
mm.
+
6.4.
2
2w
8
6.3.
0
0
Cr: 6.2-
m
c;l
4
6.1-
p:
6.
E
E9
ECr:
w
z
&
-
0
cb
n o
5.9-
0
0
5.8-
no
0%
8 0
IOMALe]
FEMALE
M
0
0
5.14
-
-
r
Fig. 2. AZouatta senicdus. A plot of In inner biorbital breadth vs. In basicranial length. As in most comparisons, growth series for males and females are coincidental such that individuals of both sexes lie along a common
scaling trajectory. In of 1*10-' mm.
degree of sexual dimorphism in the hyoid apparatus of this species and the effects
of sexual selection on functionally associated structures [Cole, 1990; Crockett &
Eisenberg, 1986; Hershkovitz, 1949; Schultz, 1960; Thorington et al., 19791.
Mantled Howler Monkey Comparisons
In Alouatta palliata, all bivariate regressions vs. basicranial length are highly
correlated (Table I). Regression coefficients range from strong negative allometry
for neurocranial volume and bitemporal breadth to strong positive allometry for
6.6.
0
6.5.
C
B
8
6.4.
6.3.
6.2.
0
&RJ
6.1.
8 8"
6-
0
0
08
5.9-
FEMALE
0
5.8-
0
0
5.1i
Fig. 3. Alouatta seniculus. A plot of In bicondylar breadth vs. In basicranial length. In this case, the common
ontogenetic pattern for males and females is slightly curvilinear, which is atypical for most plots of the howler
data in log-log space. In of 1*10-' mm.
2a
L
0
1.5.
10
0
.5-
E
0
0
0
0-
5
0
c -1.
E
0
OMA ALE I
-1.5.
-2.
0
-2.5.
.5
.
.
1
-
-
1.5
-
.
2
25
3
3.5
4
4.5
5
,
5.5
Fig. 4. Alouattu seniculus. A plot of PCA Factor I scores vs. dental age based on 31 cranial variables. This
illustrates the multivariate pattern of sexual differentiation in red howlers.
286 I Ravosa and Ross
TABLE 11. Between-Sex t Tests at Each Dental Age*
Variable"
Alouatta seniculus
males vs. females
Upper face height
Lower skull length
Bicanine breadth
P3 bite point length
M2 bite point length
Symphysis height
Symphysis width
Medial pterygoid lever arm length
Postorbital bar width
Palate length
Upper palate breadth
Bizygomatic breadth
Orbital volume
Browridge height
Outer biorbital breadth
Inner biorbital breadth
Orbit width
Basicranial length
Zygomatic arch height
Masseter lever arm length
Temporalis lever arm length
Temporal fossa length
Ramus height
M2 corpus height
M2 corpus width
Bieondylar breadth
Bicoronoid breadth
Bipterygoid breadth
Bigonial breadth
Zygomatic arch width
Orbit height
Neurocranial volume
Interorbital breadth
Bitemporal breadth
Postcanine toothrow length
Body weight
*Dental ages 1-5: cases where male measures are significantly larger than females are noted in hold; t test, P
< 0.05.
"Variables are ranked in descending order by the dental age a t which A . seniculus sexual differences are
statistically significant.
ramus height and mandibular corpus height, which is similar to results for red
howlers. Between-sex comparisons of allometric growth trajectories for A. palliata
are not significant in 29 of 33 cases, which likewise demonstrates a strong pattern
of ontogenetic scaling of cranial proportions (Table I; Figs. 5-7). Thus, in mantled
howlers, most morphological differences between adults of each sex are also due to
the differential extension of common patterns of relative growth.
T tests a t dental ages 1 and 2 between cranial measures for male and female
A. palliata are not significantly different (Table IT). At dental age 1 most female
means exceed the means for males (Table 111; see also Fig. 81, much as demonstrated in red howlers at dental age 2. However, at dental age 2 the pattern of
Cranial Growth and Scaling in Howler Monkeys / 287
TABLE 111. Percentages for the Number of Cranial
Measures Where Male Means Exceed Female Means and
Female Means Exceed Male Means
Species
Alouatta seniculusb
Alouatta palliatab
Dental age
1
2
3
4
5
1
2
3
4
5
Cranial measures
malesifemales"
979613%
3696164%
97%/3%
86%/11%
979613%
1996/81%
97%13%
83%/14%
94%/68
97%!3%
"Percentages do not always add up to 100%for A. seniculus and A. palliata
due to cases where both sex means are equal.
bNote that for A . seniculus it is a t dental age 2 that female measures have
the greatest tendency to exceed male measures, whereas for A. palliata it
is at dental age 1 that female measures have the greatest tendency to
exceed male measures.
sexual size differentiation in mantled howlers is reversed, with the vast majority
of means for male cranial measures exceeding the means for female dimensions;
this pattern continues through adulthood and is also indicated by the multivariate
analyses of sexual growth and differentiation (Fig. 8). At dental age 3, only 1of 36
t tests is significant. On the other hand, at dental age 4, 7 of 36 cases are significantly different. At dental age 5, t tests between cranial measures for adult males
and females are significant in 33 of 36 comparisons, with males being consistently
larger in size. In the remaining three cases, male dimensions are not significantly
larger than those for females.
In A . palliata, ranked dimorphism ratios of 36 cranial dimensions indicate that
neurocranial volume (32nd of 36) and postcanine toothrow length (35th of 36) have
two of the lowest values (Table IV), again much as predicted by the apparent
dissociation of brain size and postcanine tooth size from selection for body-size
differences between the sexes. Body weight for mantled howlers has a very high
dimorphism ratio (2nd of 361, which is similar to t h a t for red howlers. Of those
structures associated with the hyoid apparatus, only ramus height has a very high
value (5th of 361, which might be expected due to a lesser amount of dimorphism
in the hyoid complex of this taxon [Crockett & Eisenberg, 1986; Hershkovitz, 1949;
Schultz, 1960; Thorington et al., 19791.
Red and Mantled Howler Monkey Comparisons
Given the pervasive pattern of ontogenetic scaling of cranial proportions in
each howler monkey species, additional analyses were performed to examine if
both taxa share common patterns of relative growth. In 24 of 33 bivariate comparisons, Alouatta seniculus and A . palliata, in fact, do show a pervasive pattern of
ontogenetic scaling (Table V; Figs. 9, 10). However, in seven cases the regression
line for mantled howlers is transposed above that for red howlers (e.g., Fig. 11) and
in two comparisons the data for red howlers are transposed above those for inantled
howlers. Several of the dimensions where the A . palliata data scatter is transposed
above that for A. seniculus interestingly relate to the masticatory apparatus: bi-
288 I Ravosa and Ross
zygomatic breadth, zygomatic arch height and width, mandibular corpus width,
and symphysis width (e.g., Fig. 11).
DISCUSSION
Allometry and Sexual Differentiation in Howler Monkeys
Comparisons of male and female red howler regression lines strongly suggest
that morphological differences between adults of each sex result from the extension of common patterns of relative growth to larger adult male skull size (Table
I; Figs. 1-3). T tests for AEouattu seniculus indicate that males and females have
similar infant sizes (Table 11). If the smaller overall adult size and ontogenetic
trajectory of female red howlers is considered primitive, the growth pattern for
males follows the prediction for rate hypermorphosis because significant differences in the mean size of cranial measures become expressed with greater frequency in the later stages of ontogeny. The ontogenetic development of such differences apparently occurs early, since by dental age 3 most male measures at least
demonstrate a trend towards being larger than those for females (Table 111; see also
Fig. 4).In A. seniculus, a greater number of sexual comparisons are significant a t
dental age 3 than occurs in A . palliata, which suggests that perhaps rate hypermorphosis has been more important in the evolution of sexual dimorphism in red
howler monkeys than in mantled howlers. However, since morphological differences between adults are greater than differences between subadults, time hypermorphosis is also apparently important in the development of sex dimorphism in
A. seniculus (see also Fig. 4).
This conclusion about significant sexual bimaturism is supported by data on
free-ranging A. seniculus indicating that sexual maturity takes place a t approximately 48.5 months for females and 62 months for males [Crockett & Sekulic,
19821. Therefore, it appears that in terms of time hypermorphosis, sexual maturation patterns in the cranium of A. seniculus correspond to field data on sexual
maturation patterns [cf. Crockett & Sekulic, 19821, but this may not be the case in
terms of rate hypermorphosis. These discrepancies might highlight different sexual dimorphisms Lsensu Oxnard, 19831 being expressed a t different times during
ontogeny, such that data on craniodental maturation may not always reflect patterns of somatic and behavioral development. For example, physically mature
howlers, especially males, are not necessarily socially mature adults [Crockett &
Eisenberg, 19861. The potential for such discrepancies should be accorded greater
attention in future studies of growth and sexual dimorphism.
Comparisons of male and female mantled howler regression lines likewise
suggest that morphological differences between adults of each sex result from the
extension of common patterns of relative growth t o larger adult male skull size
(Table I; Figs. 5-7). 7'-tests for Alouatta palliata indicate that males and females
have roughly similar infant sizes (Table 11).By dental age 2, however, most male
measures are (not significantly) larger than those for females (Table 111; see also
Fig. 8). If the smaller overall adult size and ontogenetic trajectory of female mantled howlers is considered primitive] the growth pattern for males follows the
prediction for rate hypermorphosis because significant differences in the mean size
of cranial measures become expressed with greater frequency in the later stages of
ontogeny. While this suggests that male-female differences in mantled howlers
perhaps occur earlier in ontogeny than in red howlers, in fact red howlers exhibit
a greater number of significant sexual differences at dental age 3. Because morphological differences between adult mantled howlers are especially marked visa-vis differences between subadults, this pattern suggests that time hypermorpho-
Cranial Growth and Scaling in Howler Monkeys / 289
TABLE IV. Ranked Adult Sexual Dimorphism Ratios
Variable"
Zygomatic arch width
Bigonial breadth
Ramus height
Postorbital bar width
Browridge height
Symphysis width
Medial pterygoid lever arm letngth
Body weight
M2 bite point length
Bizygomatic breadth
M2 corpus height
Temporal fossa length
Orbital volume
Zygomatic arch height
Bicanine breadth
Masseter lever arm length
Lower skull length
P3 bite point length
Temporalis lever arm length
Basicranial length
Upper face height
Palate length
Bicondylar breadth
Symphysis height
Bicoronoid breadth
M2 corpus width
Bipterygoid breadth
Interorbital breadth
Upper palate breadth
Outer biorbital breadth
Inner biorbital breadth
Neurocranial volume
Postcanine toothrow length
Orbit width
Orbit height
Bitemporal breadth
Alouatta seniculus
maledfemales
Alouatta palliata
males/females
1.628
1.498
1.433
1.406
1.336
1.315
1.294
1.286
1.255
1.248
1.242
1.236
1.231
1.215
1.206
1.206
1.195
1.195
1.189
1.184
1.179
1.168
1.168
1.147
1.140
1.138
1.131
1.125
1.120
1.080
1.064
1.058
1.054
1.051
1.045
1.021
1.047
1.157
1.257
1.249
1.292
1.238
1.284
1.336
1.220
1.201
1.208
1.223
1.182
1.178
1.199
1.183
1.180
1.177
1.215
1.151
1.244
1.160
1.140
1.161
1.153
1.225
1.142
1.366
1.109
1.136
1.124
1.108
1.057
1.081
1.113
1.057
"Variables are ranked in descending order by the A . seniculus adult male meadadult female mean ratio;
monomorphism = 1.00. Note that A . seniculus shows a higher degree of dimorphism.
sis has also been important in the development of sexual dimorphism. The cranial
results regarding sexual bimaturism also correspond to Glander's [ 19801 study of
free-ranging A . palliatu, which found sexual maturity occurring a t about 36
months in females and 42 months in males.
Both rate and time hypermorphosis appear to have influenced the evolution of
sexual dimorphism in howler monkeys. The fact that some of the morphological
differences between the sexes are manifested later in development for mantled
howlers than occurs in red howlers suggests that perhaps time hypermorphosis has
been of greater importance in the evolution of sexual dimorphism in mantled
howler monkeys. On the other hand, rate and time hypermorphosis may have been
of more equal importance in the evolution of sexual dimorphism in red howlers.
290 / Ravosa and Ross
6.51
2Q
2p:
0
6.4-
cPoo
(DO
#Poo
6.3-
O
6.2-
Q
ma
5
&
crn
6.1.
9 0
Q
ono%
5.9.
5.8-
0
5.1.
M
0
%
I
6-
@3
-
t
F
l
El FEMALE
Q
,
5.6-
log BASICRANIAL LENGTH
Fig. 5. Alouuttu palliata. A plot of In outer biorbital breadth vs. In basicranial length. Note that the growth
trajectories for male and female mantled howlers are ontogenetically scaled. This typifies all but four bivariate
comparisons for this species. In of 1*10-' mm.
6.83
-
*
L
0
0 %@OO
6.6UQ 0
6.4-
d-
6.2-
fiV
65.85.65.4-
no
0
5.2-
m o
5-
I.....]
Q FEMALE
0
4.8-
1
Fig. 6. Alouattu palliata. A plot of In ramus height vs. In basicranial length. Again, the ontogenetic scaling
trajectories for males and females are coincidental. In of 1*10W1mm.
Additional work provides a broader basis for understanding the evolution and
expression of sexual dimorphism in howler monkeys. Thorington e t al. [19791
found that A. seniculus males show a n earlier onset of scrota1 development and
relatively larger hyoids, both of which are probably associated with their agegraded hierarchical social system. On the other hand, A. palliata males have relatively smaller hyoids and show a more prolonged period of time where their
genitalia mimic those of females. Thorington et al. 119791 suggest t h a t these aspects of sexual development in mantled howlers reflect a strategy of avoiding
male-male conflicts, such a s competition for reproductive access to females.
Red howlers differ from mantled howlers in other related aspects of their
Cranial Growth and Scaling in Howler Monkeys / 291
6~-
*
'
.
.
'
-
'
5.8-
0
&O
0
oo
0
5.6.
5.4.
W
b
z
4
5.2.
0
Em
5.
-
0%
0 s
00
co
I-ZJ
CI FEMALE
B
0
4.8.
4.6-
7
Fig. 7. Alouatta pulllata A plot of In bicanine breadth vs. In basicranial length. As in most cases, males and
females share similar patterns of relative growth In of 1*10-' mm.
2.
L
0
1.5.
0
1.
m
W
a
0
a
.5.
n
h
c1?
p:
0
6
*
E*
D
0
5:
0..
0
-.5.
0
k
-1.
-1.5.
-2.
-2.5.
.5
0
-
.
1
.
.
IS
.
.
2
.
.
25
b
3
3.5
4
4.5
5
5.5
Fig 8 Alouatta palliata A plot of PCA Factor I scores vs dental age based on 31 cranial variables This depicts
the multivariate pattern of sexual &fferentiation in mantled howlers
behavior and ecology. Alouatta seniculus have mostly unimale troops of about
4-11 individuals, whereas A . palliata live in multimale troops of 8-21 individuals
[Crockett & Eisenberg, 1986; Glander, 1980; Milton, 19801. As such, the sex ratio
292 I Ravosa and Ross
for red howlers is about 1.8 females per male, while mantled howlers have a higher
sex ratio of about 2.4 females per male [Crockett & Eisenberg, 19861. Milton [19801
also indicates t h a t red howler troops in Peru have larger home ranges than mantled howlers in Panama. On the other hand, mantled howler troops in Panama
come into contact more often than red howler troops in Peru, which may result in
higher intraspecific competition in A. palliata than in A. senicuhs [Milton, 19801.
All of these factors highlight a potential association between increased competition
levels and a n earlier onset of sexual differentiation.
Interestingly, there are some parallels between the socioecology of Alouatta
caraya, the black howler monkey, and A. seniculus, which do not characterize A.
palliata. Black howlers resemble red howlers in that males display a n early onset
of sexual differences in external morphology, such as testes descent [Crockett,
1987; Thorington et al., 19791; in having smaller, mostly unimale troops (mean of
8.9) and lower sex ratios (slightly less than 2.0) than mantled howlers [Crockett &
Eisenberg, 1986; Glander, 1980; Milton, 1980; Thorington et al., 19841; and in
being highly dimorphic in hyoid and body size. Moreover, based on body-weight
data for A. caraya, Leigh [1992] found that males mature at 90 months and females
mature a t 54 months, indicating considerable bimaturism like A. seniculus. One
manner in which red and black howlers differ is that A. caraya is the only howler
apart from A. fusca clamitans that is sexually dichromatic; in both of these taxa,
changes in male pelage occur a t puberty and are due apparently to female (epigamic) sexual selection [Crockett, 19871.
In sum, while our study primarily summarizes available information on sexual
dimorphism in the genus Alouatta, i t is evident t h a t mantled howlers differ significantly from red (and black) howlers in terms of their socioecology and patterns
of sexual differentiation. This is not overly surprising a s similar levels of intrageneric variability in the development of sexual dimorphism are noted in Macaca
[Leigh, 19921. Among howlers, it is possible that many of the selective pressures
underlying the development of sexual dimorphism and other aspects of the biology
of A. seniculus have also played a significant role in the evolution of the black
howler, A. caraya. According to Crockett & Eisenberg [19861, many of the features
shared by red and black howlers may well be primitive for the genus. Conversely,
the characteristics observed for A. palliata are supposedly more derived for howler
monkeys. Future work could focus profitably on the timing of sexual dimorphisms
as well a s the relationship between patterns of sexual differentiation and levels of
intra- and inter-sexual competition. Such data for all howler monkeys would provide greater resolution to the issues raised above.
The allometric analyses of howler cranial morphology also demonstrate the
utility of a n ontogenetic criterion of subtraction regarding neural and dental patterns of size variability. In both red and mantled howlers, low levels of dimorphism
in neurocranial size strongly supports previous claims that selection for greater
intraspecific differentiation between the sexes or subspecies has a minimal effect
on brain growth [Gould, 1975a; Lande, 1979; Ravosa, 1991a, 1992; Riska & Atchley, 1985; Shea, 1983b, 1988; Shea et al., 19871 and postcanine tooth growth [Cochard, 1985,1987; Gould, 1975b; Ravosa, 1991a, 1992; Shea & Gomez, 1988; Shea
et al., 19901 (Table IV).
Allometry and Functional Differences Between Howler Monkeys
Lastly, comparisons of ontogenetic series for red and mantled howlers shed
light on possible functional bases of species differences in skull form. While the
ANCOVAs of red and mantled howler regression lines indicate that most morphological differences between adults of each species result from the extension of
Cranial Growth and Scaling in Howler Monkeys I 293
TABLE V. Between-SpeciesANCOVAs
Variable
Browridge height
Postorbital bar width
Zygomatic arch height
Zygomatic arch width
Symphysis height
Symphysis width
Outer biorbital breadth
Inner biorbital breadth
Interorbital breadth
Orbit height
Orbit width
Upper palate breadth
Bicanine breadth
Palate length
Lower skull length
Upper face height
Bizygomatic breadth
Bigonial breadth
Bicondylar breadth
Bicoronoid breadth
Ramus height
Temporal fossa length
Bitemporal breadth
Bipterygoid breadth
P3 bite point length
M2 bite point length
M2 corpus height
M2 corpus width
Masseter lever arm length
Temporalis lever arm length
Medial pterygoid lever arm length
Orbital volume
Neurocranial volume
vs. Basicranial lengtha4
S>P**
NS
S<P*
S<P*
NS
S<P*
NS
NS
NS
S<P*
S<P*
NS
NS
NS
NS
NS
S<P*
NS
NS
NS
NS
NS
NS
S>P*
NS
NS
NS
S<P*
NS
NS
NS
NS
NS
”**Significant slope and Y-intercept differences between howler monkey
regression lines, ANCOVA, P < 0.05.
b* Significant Y-intercept differences between howler monkey growth trajectories.
‘NS, no significant differences between species, ANCOVA, P > 0.05.
dS>P,A . seniculus line transposed above; S<P, A . palluzta transposed. “S”
is A . seniculus; “ P is A . palliata.
common patterns of relative growth (Table V; Figs. 9, lo), in several cases, the data
scatter for mantled howlers is transposed above that for red howlers (e.g., Fig. 11).
One such case is bizygomatic breadth, such that at a given basicranial length, A.
palliata has a wider bizygomatic region. This could result from mantled howlers
having relatively larger temporalis muscles, and other jaw muscles as well, perhaps due to a folivorous diet with slightly higher percentages of tough, mature
leaves [Crockett & Eisenberg, 19861. Moreover, this could explain similar transpositions for both dimensions of the zygomatic arch and the width of the mandibular corpus and symphysis in A. palliata, structures which resist masticatory
stresses and would be positively influenced by the forces produced by relatively
larger jaw muscles and a tougher diet.
294 I Ravosa and Ross
-
6.46.26d
Ec
2
Iro
5.85.6-
5.4-
0
c
0
5.20
5-
-
CI@
Fig. 9. Alouatia seniculus and A . pulliata. A plot of In palate length vs. In basicranial length. Note that the
ontogenetic scaling trajectories for red howlers and mantled howlers are also coincidental. This is typical for
about three-fourths of the bivariate comparisons between these species. In of 1*10-’ mm.
6
b
5
T
CI
t
C
:v
I
5.61
0 A.PAUIATA
4AJ
1
5.8
6
6.2
6.4
6.6
6.8
log BASICRANIAL LENGTH
Fig. 10. Alouatta seniculus and A. palliata. A plot of In temporal fossa length vs. In basicranial length. Note
again that relative growth patterns for red howlers and mantled howlers are similar. In of 1-10 mm.
CONCLUSIONS
Most sexual differences in skull form within both red and mantled howler
monkeys, and to a slightly lesser extent between species, result from the differential extension of common patterns of relative growth or ontogenetic scaling. As
noted earlier, similar observations have been noted for a wide variety of primates,
which suggests that this is a “simple” genetic and developmental means of attaining sexual size differentiation in mammals. This study details the two heterochronic processes by which sexual dimorphism has apparently developed in two
howlers, namely, rate and time hypermorphosis, but, apparently, both processes
Cranial Growth and Scaling in Howler Monkeys / 295
m
P
5
8h
1z
-
M
0
4.8.
4.6:
4.44.2:
0
0,
4.
0 A.PALWATA
0
3.83.6J
5.8
6
6.2
6.4
6.6
log BASICRANIAL LENGTH
6.8
1
Fig. 11. AZouatta seniculus and A. pall&a. A plot of In symphysis width vs. In basicranial length. In this case,
the ontogenetic scaling trajectory for red howlers is transposed below t h a t for mantled howlers. This occurs in
about one-fourth of all bivariate comparisons (see text for discussion). In of 1*10-' mm.
occur to different extents within each species. Results for both monkeys indicate
that selection for sexual size differentiation has a minor effect on brain size and
postcanine tooth size dimorphism. Comparisons of allometric trajectories for red
and mantled howlers further demonstrate a strong pattern of ontogenetic scaling
of cranial proportions, with some scaling differences perhaps related to variation in
diet and masticatory function.
ACKNOWLEDGMENTS
We thank S. Leigh, B. Shea, K. Glander, and a n anonymous reviewer for
helpful comments and suggestions. For access to howler cranial collections, thanks
are offered to K. Milton (University of California-Berkeley); G. Musser and W.
Fuchs (American Museum of Natural History); R. Thorington and L. Gordon (National Museum of Natural History); B. Patterson, L. Heaney, W. Stanley, and J.
Kerbis (Field Museum of Natural History); and M. Rutzmoser (Museum of Comparative Zoology). E. Fox is thanked for help with various phases of this project.
This research was supported in part by NIH (DE-05595) and NSF (BNS-8813220)
grants to MJR as well a s a n AMNH collection study grant to CFR. Both MJR and
CFR were also supported by the Department of Biological Anthropology and Anatomy, Duke University Medical Center. Many Alouatta palliatu crania used in this
study were collected by K. Milton under the support of NSF grant BNS-8512634.
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APPENDIX
Craniodental Measurements
Basicranial length: nasion to basion
Lower skull length: prosthion to basion
Palate length: prosthion to posterior nasal spine
Upper face height: prosthion to nasion
Outer biorbital breadth: frontomalare temporale to frontomalare temporale
Inner biorbital breadth: frontomalare orbitale to frontomalare orbitale
Orbit height: greatest vertical distance between the inner aspect of the superior
and inferior orbital rims perpendicular to outer biorbital height
Orbit width: greatest horizontal distance between the inner aspect of the medial
and lateral orbital rims parallel to outer biorbital height
Interorbital breadth: maxillofrontale to maxillofrontale
Upper palate breadth: between outer superior alveolar M1 junctions
Bizygomatic breadth: between the outer lateral surfaces of the zygomatic arches
Symphysis height: infradentale to the inferior border of the symphysis
Symphysis width: perpendicular to symphysis height, labiolingually
Mandibular corpus height: alveolus at M2 t o inferior border of the lower jaw
Mandibular corpus width: perpendicular to M2 corpus height, buccolingually
Ramus height: superior condylar surface to gonion
Bigonial breadth: gonial angle to gonial angle
Bicondylar breadth: between the outer lateral condylar surfaces
Bicoronoid breadth: between the lateral aspects of the coronoid processes’ tips
Masseter lever arm length: inner superior surface of the external auditory meatus
to the anterior root of the zygomatic arch
Temporalis lever arm length: with jaws in occlusion, inner superior surface of the
external auditory meatus to the anterior surface of the coronoid process tip
Medial pterygoid lever arm length: inner superior surface of the external auditory
meatus to the anteriormost point at the junction of medial and lateral pterygoid plates
M2 bite point length: inner superior surface of the external auditory meatus to the
anterior mesial alveolar surface of the upper M2
P3 bite point length: inner superior surface of the external auditory meatus to the
anterior mesial alveolar surface of the upper P3
Browridge height: orbital mid-point perpendicular to the inner inferior surface of
the superior orbital rim
Postorbital bar width: mediolaterally and horizontally just below frontomalare
orbitale
Bitemporal breadth: minimum breadth between the temporal fossae across the
braincase
Temporal fossa length: antero-posterior measure from the masseteric tubercle a t
the inferior zygomaticomaxillary suture to the inner surface of the zygomatic
process of the temporal
Zygomatic arch height: height of the zygomatic arch at the zygomaticotemporal
suture
Cranial Growth and Scaling in Howler Monkeys / 299
Zygomatic arch width: width of the zygomatic arch at the zygomaticotemporal
suture
Bicanine breadth: between the outer lateral surfaces of the canine alveolus at the
the junction of the canine and alveolus
Bipterygoid breadth: between the outer lateral surfaces of the lateral pterygoid
plates
Postcanine toothrow length: mesial alveolar junction of anterionnost premolar to
the distal alveolar junction of t,he posteriormost molar
Orbital volume: filled to the orbital aperture with barley to the nearest half cc
Neurocranial volume: filled to the foramen magnum with barley to the nearest cc
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