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Craniodental mechanics and diet in Asian colobines Morphological evidence of mature seed predation and sclerocarpy.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:137–148 (2010)
Craniodental Mechanics and Diet in Asian Colobines:
Morphological Evidence of Mature Seed Predation
and Sclerocarpy
Daisuke B. Koyabu1,2* and Hideki Endo1
1
2
The University Museum, The University of Tokyo, Tokyo 114-0033, Japan
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 114-0033, Japan
KEY WORDS
ecomorphology; masticatory apparatus; bite force; seed eating
ABSTRACT
Folivory has been accepted as the general dietary pattern for colobines. However, recent ecological studies have revealed that extensive seed eating
is found in some colobine species. The ripeness of
foraged seeds is also reported to differ between seed eaters. As seeds are generally stress-limited and may pose
greater mechanical demands, seed-eating species are
predicted to exhibit morphological features adaptive for
seed predation. In addition, species that feeds on seeds
from unripe fruits with hard pericarp is predicted to
exhibit increased leverage for anterior dentition. To test
these hypotheses, we compared the craniodental morphology of seed-eating Asian colobines (Presbytis rubicunda and Trachypithecus phayrei) with those of species
that rarely exploit seeds (Presbytis comata, Trachypithecus obscurus, and Semnopithecus vetulus). The results
show that the seed-eating colobines possess a masticatory system with enhanced leverage at postcanine bite
points. The sclerocarpic forager P. rubicunda also exhibits markedly greater masticatory leverage at anterior dental bite points, while the mature-seed-eating T. phayrei
shows no such advantage for canine and incisor use.
These observations suggest that P. rubicunda is well
adapted to husking the resistant pericarps of unripe
fruits, using the anterior dentition and to gain access to
the immature seeds, whereas such sclerocarpic feeding
behavior may be less important for T. phayrei. Our findings indicate that the distinctive craniodental variations
of colobines may be linked to mature and/or immature
seed eating and suggest the significance of seed predation for the evolution of colobine monkeys. Am J Phys
Anthropol 142:137–148, 2010. V 2010 Wiley-Liss, Inc.
Primates in the subfamily Colobinae have long been
recognized to share a suite of morphological adaptations
to folivory when compared to members of their more frugivorous sister taxa, the Cercopithecinae (Hylander,
1979; Radinsky, 1985; Bouvier, 1986a; Ravosa, 1990;
Oates and Davies, 1994). Morphological traits of the
Colobinae such as relatively sharp molar crests, thin
tooth enamel, longer molar rows, smaller incisors, robust
mandibles, and underbite have been considered adaptations for masticating leaves (Hylander, 1975, 1979;
Teaford, 1983a; Ravosa, 1990, 1996; Lucas and Teaford,
1994). However, recent ecological studies have demonstrated that dietary patterns differ considerably among
the colobine taxa. In particular, seed eating has emerged
as an important behavior of some colobine species
(Curtin, 1976; McKey, 1978; McKey et al., 1981; Davies
et al., 1988, 1999; Davies, 1991; Bennett and Davies,
1994; Dasilva, 1994; Maisels et al., 1994; Oates and Davies, 1994; Waterman and Kool, 1994; Daegling and
McGraw, 2001; Chapman et al., 2002). Previous studies
have suggested that when preferred young leaves are in
short supply, some species fall back on other food resources (Struhsaker, 1975; Oates, 1977; McKey et al., 1981;
Yeager, 1989; Davies, 1991; Bennett and Davies, 1994;
Oates and Davies, 1994). On the other hand, considerable craniodental variations exist within colobine monkeys (Schultz, 1958; Verheyen, 1962; Leutenegger, 1971;
Swindler and Orlosky, 1974; Hull, 1979; Teaford, 1983b;
Lucas and Teaford, 1994; Pan et al., 1995; Hayes et al.,
1996; Jablonski et al., 1998; Daegling and McGraw,
2001; O’Higgins and Pan, 2004; Pan and Groves, 2004;
Willis and Swindler, 2004; Pan, 2006), and it appears
from the degree of craniodental variation among Asian
colobines that various different foods fill the role as fall
back resources. The functional significance of the craniodental variations of colobine monkeys and the evolutionary factors driving this morphological variation are
poorly understood (Daegling and McGraw, 2001; Pan,
2006; Koyabu and Endo, 2009).
Among African species, seed-eating colobines have
been found to possess a more mechanically efficient masticatory structure compared to colobines that mainly eat
young leaves, suggesting functional adaptation for feeding on stress-limited foods (Koyabu and Endo, 2009).
Whether this ecomorphological dichotomy can be
extended to Asian colobines is not yet clear. Here, we
use dietary information to predict patterns of masticatory muscle leverage among five species of Asian leaf
C 2010
V
WILEY-LISS, INC.
C
Grant sponsors: Japan Society for the Promotion of Science
(Research Fellowship for Young Scientists to DBK; Core-to-Core
Program HOPE Grant 15001 to Primate Research Institute, Kyoto
University); Ministry of Education (Grants-in-Aid for Scientific
Research to HE).
*Correspondence to: Daisuke B. Koyabu, The University Museum,
The University of Tokyo, Tokyo 114-0033, Japan.
E-mail: koyabu@um.u-tokyo.ac.jp
Received 19 February 2009; accepted 18 September 2009
DOI 10.1002/ajpa.21213
Published online 20 January 2010 in Wiley InterScience
(www.interscience.wiley.com).
138
D.B. KOYABU AND H. ENDO
monkeys (Presbytis rubicunda, P. comata, Semnopithecus
vetulus, Trachypithecus obscurus, and T. phayrei).
Dietary variation among Asian colobines
To develop testable morphological hypotheses, we
reviewed the literature on Asian leaf monkey feeding
ecology (see Table 1 for a summary of feeding frequencies for the diet reviewed). Young leaves are the most
frequently foraged food item for P. rubicunda (37% of the
annual diet) at Sepilok Forest, North Borneo, but the
diet of this species is also characterized by a high intake
of seeds (30%; Davies, 1991). In August, when young
leaves become scarce, as much as 87% of feeding time is
dedicated to seed predation (Davies, 1991). As Davies
(1991) has described, most seeds are ‘‘bitten, chewed,
swallowed, and digested, leaving no chance for survival.’’
P. rubicunda predates pyrenes of Eusideroxylon zwageri
and legume seeds such as Intsia palembanica and Milletia (Davies, 1991). P. rubicunda also feeds on seeds of
unripe fleshy Litsea fruits, occasionally discarding the
pericarp and mesocarp (Davies, 1991). In the case of T.
phayrei at Gumti in northeast India, young leaves comprise the major part of the annual diet (49%), but seeds
are also an important food source (23%; Gupta and
Kumar, 1994). In particular, seeds are eaten more extensively in January (43%), February (50%), and March
(70%), when young leaves become less abundant (Gupta
and Kumar, 1994). Fleshless legume seeds of Albizzia
lebbek and A. procera are found to be the most extensively foraged species (Gupta and Kumar, 1994). Similarly, a whole-year study on T. phayrei at Phu Khieo in
Thailand reported that seeds form a substantial part of
this primate species’ diet (22%), in which legumes were
the most frequently consumed seeds (Suarez, 2006).
While P. rubicunda and T. phayrei are considered predominantly seed predators (Davies, 1991; Gupta and
Kumar, 1994), seed eating is rarely found in P. comata,
T. obscurus, and S. vetulus. At Kuala Lompat in Malaysia, T. obscurus has been reported to feed selectively on
young leaves (36%) or on fruits (32%), but rarely on
seeds (3%), throughout the year (Curtin, 1976). In the
case of P. comata of West Java, more than half of the annual feeding time is spent on young leaves (59%),
whereas seeds and mature leaves are rarely eaten (1
and 6%, respectively; Ruhiyat, 1983). Field studies on S.
vetulus in Panadura and Piliyandala, Sri Lanka, have
shown that fruits (averaging 53%) and young leaves
(19%) dominate the annual diet, while seeds and mature
leaves are less important (4 and 6%, respectively; Dela,
2007). S. vetulus has been reported to show preference
for young leaves, which are presumably rich in protein
and less lignified (Hladik, 1977), and fruits that are easily digestible and contain energy-rich sugars (Dela,
2007).
Food property and predictions of masticatory
apparatus based on the dietary findings
Seeds can be an important food item for primates, as
they are generally highly nutritious (van Roosmalen
et al., 1988). Protein is found to be highly concentrated
in some seeds, particularly in those of Leguminosae,
which are frequently exploited by colobines (Davies,
1991; Gupta and Kumar, 1994; Waterman and Kool,
1994). In addition, seeds are a rich source of starch and
lipids (Waterman and Kool, 1994). Field studies also supAmerican Journal of Physical Anthropology
port that seeds are selected by colobines particularly for
their high concentration of protein and/or lipids (e.g.,
McKey et al., 1981; Davies et al., 1988; Maisels et al.,
1994). While seeds can be a desirable source of nutrition,
they are often protected by resistant shells (Lucas and
Teaford, 1994; Lucas et al., 2000, 2002). These seed
shells are highly dense woody tissues composed of thick
cell walls that purely function as protector against predation (Lucas and Peters, 2000). The fibers of many
mature seed shells have a cell-wall volume fraction more
than 90% and a maximal microhardness of about 300
MPa (Lucas et al., 2000). Thus, mature seed shells are
generally highly resistant to crack initiation and exhibit
limited strain at high stress before crack formation, i.e.,
they are stress-limited (Lucas, 2004b). Therefore, mature
seeds require stronger bite force to fracture compared to
other less resistant items such as pulpy ripe fruits
(Lucas et al., 2000, 2002; Teaford and Ungar, 2000).
Hypothesis 1: Leaf monkeys that consume a high
proportion of seeds from mature fruits will exhibit
increased leverage along the cheek tooth row. Given
that P. rubicunda and T. phayrei feed extensively on
mature seeds, which are generally postulated to be
mechanically resistant, we hypothesize that these species are capable of generating relatively greater bite
forces along the postcanine tooth row, where the masticatory muscle force can be recruited most efficiently.
In contrast, a strong bite force may not provide an
advantage to P. comata, T. obscurus, and S. vetulus
when foraging.
While mature seeds are foraged by both P. rubicunda
and T. phayrei, unripe ones are also foraged frequently
by the former (Davies, 1991; Gupta and Kumar, 1994;
Suarez, 2006). Unripe seeds are generally less crushingresistant and less toxic than ripe ones, since mechanical
resistance of seed shells and concentration of secondary
compounds such as tannins increase with maturation
(Ayres, 1986; Kinzey, 1992). However, puncture resistance of outer husks of unripe fruits is often much higher
than that of ripe fruits. Among the New World primates,
Pitheciinae have a substantial portion of seeds in their
diet (Ayres, 1989; Kinzey and Norconk, 1990, 1993;
Kinzey, 1992). Although both Chiropotes and Pithecia
frequently predate seeds, the crushing resistance and
ripeness of foraged seeds differ significantly between the
two pitheciine genera (Kinzey, 1992; Kinzey and Norconk, 1993). Chiropotes collects immature seeds from
unripe fruits, which have pericarps of higher puncture
resistance, whereas Pithecia feeds more frequently on
ripe seeds, which have higher resistance to crushing but
are not protected by puncture-resistant pericarps
(Kinzey and Norconk, 1993). Chiropotes uses its anterior
dentition to remove the puncture-resistant husks of
unripe fruits and gain access to the immature seeds, a
behavior referred as sclerocarpic harvesting (Kinzey and
Norconk, 1993). On the other hand, Pithecia crushes
more resistant seeds mainly with its postcanine dentition (Kinzey, 1992). Given that P. rubicunda is found to
feed extensively on immature seeds as seen in Chiropotes, employment of the anterior dentition should be
important in P. rubicunda to scrape off the resistant
husks of unripe fruits and gain access to the seeds.
Hypothesis 2: The most sclerocarpic species will
exhibit increased leverage for incision and canine
use. Since foraging on unripe seeds may require high
139
CRANIODENTAL MECHANICS IN ASIAN COLOBINES
TABLE 1. Proportions of the annual diet of each species represented by each food class
f
Total months of observation
Young leaves
Mature leaves
Fruits
Unripe fruits
Ripe fruits
Seeds
Flowers
Others
P. comataa
P. rubicundab
S. vetulusc
T. obscurusd
T. phayreie
33
59.1
5.6
13.5
–
–
0.7
7.0
14.1
13
36.5
1.1
19.2
–
–
30.1
11.1
2.0
32
19.1
5.9
53.1
–
–
3.8
5.8
12.3
8
35.6
22.5
31.8
–
–
3.4
6.8
0.0
8
48.5
0.1
6.7
5.2
1.5
23.2
–
20.6
a
Ruhiyat (1983).
Davies (1991).
c
Dela (2007).
d
Curtin (1976).
e
Gupta and Kumar (1994).
f
Total months of observations conducted for each species.
b
Fig. 1. Diagram showing the constrained lever model of the masticatory apparatus (Greaves, 1978; Spencer, 1999). (A) Occlusal
view of the mandible showing the dental regions defined by the constrained lever model [redrawn after Spencer (1999)]. (B) Biting
at the teeth within Region I. The triangle of support is defined by the working- and balancing-side TMJs and the bite point. The
midline muscle resultant force is enclosed within the triangle of support. (C) Biting at the teeth within Region II. The midline muscle resultant force falls outside of the triangle of support as bite point shifts posteriorly. Under the classic lever model, forceful biting is predicted to involve simply posterior migration of dentition and anterior migration of masticatory muscles. However, either
anterior migration of masticatory muscles or posterior migration of dentition may provoke distraction of balancing-side TMJ, since
such change could cause the midline muscle resultant force to fall outside the triangle of support (Greaves, 1978; Spencer, 1999).
Therefore, the constrained lever model predicts that compensatory shortening of the molar row is necessary to avoid pushing distal
molars into the posterior region of the mandible (Spencer, 1999).
bite forces at the anterior dentition, we predict that P.
rubicunda, which is the most sclerocarpic forager, should
exhibit higher mechanical advantage at anterior dental
bite points than other species.
To test these hypotheses, we employ the biomechanical
approach derived from the constrained lever model
developed by Greaves (1978) and subsequently refined
by Spencer (1998, 1999) (see Fig. 1). Under the classic
lever model, forceful biting is predicted to involve simply
posterior migration of dentition and anterior migration
of masticatory muscles (e.g., Du Brul, 1977; Osborn,
1987; Ravosa, 1990; Herring, 1993). Posterior migration
of dentition may increase the mechanical advantage of
the teeth, but may potentially provoke injurious distractive forces at the balancing-side temporomandibular
joint (TMJ; Greaves, 1978; Spencer and Demes, 1993;
Spencer, 1998, 1999). Under the constrained lever model,
spatial arrangement of the masticatory apparatus is considered to be constrained by the need to avoid TMJ distractions. For the bite points enclosed roughly within
Region I (i.e., incisors, canines, and premolars; see Fig.
1A), predictions are comparable to those of the classic
lever model. Posterior migration of the dentition and/or
anterior migration of the masticatory muscles are predicted to increase the mechanical advantage of biting
(Spencer, 1999). However, as either of these changes
would alter the relative masticatory geometry, additional
mechanical consequences are expected by the constrained lever model. Since either anterior migration of
masticatory muscles or posterior migration of dentition
could cause the midline muscle resultant force to fall
outside the triangle of support defined by the TMJs and
the bite point, compensatory shortening of the molar row
is necessary to avoid pushing distal molars into the posterior region of the mandible, where TMJ distraction is
American Journal of Physical Anthropology
140
D.B. KOYABU AND H. ENDO
inevitable (Hylander, 1977; Spencer, 1998, 1999). Furthermore, since balancing-side muscle activity decreases
as bite point shifts posteriorly during mastication, additional posterior dental migration may provide little
advantage for generating greater bite force (Spencer,
1999). As such, the constrained lever model predicts that
selection for increased postcanine bite forces should
involve more medially positioned tooth rows relative to
biarticular breadth, which allows more balancing-side
muscle force to be produced during forceful biting without producing TMJ distraction (Spencer, 1999).
In sum, if the craniodental morphologies of P. rubicunda and T. phayrei are principally adapted for forceful
chewing, these species should possess relatively greater
mechanical advantages along the postcanine, reduced
molar rows, and more medially positioned tooth rows relative to biarticular breadth, compared to P. comata, T.
obscurus, and S. vetulus, species that rarely predate
seeds. Furthermore, the most sclerocarpic P. rubicunda
is predicted to exhibit greater masticatory leverage at
the anterior dental bite points. In this study, conducting
Fig. 2. Measurements employed in this study. See text for
details.
shape analysis and mechanical advantage analysis,
we evaluate whether craniodental morphological variation in Asian colobines is related to diet. This investigation aims to provide insight into the evolution of seed
eating in colobine monkeys and aid in functional interpretation of the diversity of craniofacial morphology
among primates.
MATERIALS AND METHODS
Samples and measurements
Samples included the crania of five colobine species:
P. comata (n 5 10), P. rubicunda (n 5 10), S. vetulus (n
5 12), T. obscurus (n 5 18), and T. phayrei (n 5 16). All
specimens were wild-shot adult males with full dental
eruption housed at the British Museum of Natural History (BMNH), National Science Museum, Tokyo (NSMT),
or the Zoological Reference Collection, National University of Singapore (ZRC). Only males were examined,
since too few female specimens precluded their inclusion
and that male sample sizes were large enough to avoid
biasing the sample toward more mature and possibly
hypermorphic males. Information on the specimens is
provided in the Appendix.
The measured craniodental landmarks are based on
those reported by Spencer (1999) and are illustrated in
Figure 2. Coordinates of anatomical landmarks were collected using Microscribe 3DX digitizer (Immersion Corp.,
San Jose, CA). To adjust the vertical difference in occlusal plane and TMJ, measurements were taken as projections onto the occlusal plane, defined by the point
between central incisors and right and left centers of the
trigon basin of M1 [see Spencer and Demes (1993) and
Wright (2005)]. Measurements were also projected onto
the sagittal plane to adjust the horizontal difference in
occlusal plane and TMJ. Positions of muscle origin were
measured for adductor masticatory muscles (masseter,
temporalis, and medial pterygoid muscles). Following
Spencer and Demes (1993), it was assumed that the distance from the articular eminence to the position of muscle origin should reflect the moment arm length of that
muscle. Masseter muscle position was measured as the
distance from the center of the articular eminence to the
inferior edge of the malar at the most anterior point of
attachment of the superficial masseter muscle. Temporalis muscle position was defined as the distance from the
center of the articular eminence to frontotemporale.
Medial pterygoid muscle position was estimated as the
distance from the center of the articular eminence to
pterygopalatine suture at the posterior edge of palatine.
Bite-point positions were measured from the center of
TABLE 2. Means and standard deviations (in parentheses) of measurements for each species
Measurement
Masseter position
Medial pterygoid position
Temporalis position
Biarticular breadth
Bilateral M1 breadth
Incisor—articular eminence distance
Canine—articular eminence distance
P3—articular eminence distance
M1—articular eminence distance
Molar row length
P. comata
30.24
26.09
14.07
55.86
24.74
58.59
52.10
47.34
37.20
16.31
American Journal of Physical Anthropology
(2.09)
(2.13)
(2.26)
(2.48)
(0.61)
(2.78)
(1.78)
(2.21)
(1.84)
(0.33)
P. rubicunda
32.83
28.08
14.67
57.65
23.71
58.07
51.75
47.07
36.24
15.64
(2.31)
(1.18)
(1.49)
(1.58)
(1.08)
(2.05)
(1.75)
(1.84)
(1.88)
(0.32)
S. vetulus
34.54
27.39
15.44
61.65
25.88
68.62
61.40
55.22
44.20
19.56
(3.19)
(2.70)
(1.84)
(3.84)
(1.76)
(5.19)
(3.50)
(4.89)
(4.73)
(0.67)
T. obscurus
38.46
30.21
16.28
65.24
27.03
71.29
63.46
56.17
45.36
18.86
(2.80)
(2.44)
(2.02)
(2.65)
(1.27)
(3.47)
(3.24)
(3.14)
(3.17)
(0.61)
T. phayrei
35.69
32.08
16.19
63.75
27.45
69.91
62.80
56.07
45.09
19.52
(1.47)
(1.80)
(1.26)
(3.08)
(1.23)
(2.64)
(2.08)
(2.20)
(1.97)
(1.02)
141
CRANIODENTAL MECHANICS IN ASIAN COLOBINES
1
TABLE 3. Geometric means, shape ratio means, and ratios of bilateral M breadth against biarticular breadth for each species
Measurement
P. comata
P. rubicunda
S. vetulus
T. obscurus
T. phayrei
32.94
33.62
37.07
37.69
38.77
versus Geometric mean
Masseter position
Medial pterygoid position
Temporalis position
Biarticular breadth
Bilateral M1 breadth
Incisor—articular eminence distance
Canine—articular eminence distance
P3—articular eminence distance
M1—articular eminence distance
Molar row length
0.94
0.80
0.44
1.73
0.75
1.80
1.59
1.45
1.15
0.50
1.00
0.83
0.44
1.74
0.72
1.76
1.57
1.43
1.13
0.48
0.92
0.77
0.44
1.68
0.69
1.85
1.65
1.48
1.19
0.52
0.93
0.80
0.43
1.70
0.70
1.85
1.65
1.48
1.19
0.50
0.98
0.82
0.42
1.70
0.71
1.85
1.65
1.45
1.18
0.48
versus Biarticular breadth
Bilateral M1 breadth
0.44
0.40
0.44
0.43
0.41
Geometric mean
the articular eminence to the center of the trigon basin
of M1 and P3, to the tip of the canine and to the point
between the central incisors. Biarticular breadth was
measured between the right and left centers of the articular eminence. Breadth of tooth rows was measured
between right and left centers of the trigon basin of M1.
Molar row length was measured as the linear distance
from the anterior tip of M1 to the posterior tip of M3
(Martin and Knussmann, 1988).
Mechanical and shape analyses
The mechanical efficiency of the masticatory apparatus
was compared among the five Asian colobine species. The
mechanical advantage of biting was calculated as the ratio
of the muscle position and the bite-point position (Demes
and Creel, 1988; Koyabu and Endo, 2009). Relative leverage estimations performed by regressing natural logtransformed bite point positions against natural log-transformed masticatory muscle positions (e.g., Wright, 2005)
were not applied in this study. While there is notable difference in skull size between the smaller langurs (Presbytis) and the larger langurs (Semnopithecus and Trachypithecus), those of P. comata and P. rubicunda are nearly
comparable, and those of S. vetulus, T. obscurus, and
T. phayrei are also similar with one another (Table 3). In
cases of such biased size distribution, bivariate regression
approach should be avoided, since it may amount to twopoint regressions, producing unreliable regression slopes
and residuals. Tooth row breadth relative to biarticular
breadth was assessed by the ratio of bilateral M1 breadth
against biarticular breadth. In addition to assessing
mechanical advantages, we also examined the relative
length of each linear measurement against the skull size,
to analyze the craniodental shape variation in the five
colobines. Skull size was estimated by calculating the geometric mean of all linear measurements for each specimen
(Jungers et al., 1995), and then each raw measurement
was divided by the geometric mean (Darroch and Mosiman, 1985). This method corrects for isometric size effects
(but does not correct allometric effects) and allows interspecific comparisons of relative length of each measured
trait (Jungers et al., 1995). The Mann–Whitney U test
was conducted to assess interspecifc differences, using
SPSS 11.0J (SPSS, Chicago, IL).
RESULTS
Table 2 summarizes the descriptive statistics of raw
measurements, and Table 3 shows the geometric means
of ten measurements and the relative length of each
measurement. The results of pairwise significance tests
for differences are provided in Table 4.
Figures 3–5 show the box plots of mechanical advantage for each muscle at various bite points. The leverages
for the masseter at P3 and M1 were significantly greater
in P. rubicunda and T. phayrei compared to P. comata, S.
vetulus, and T. obscurus (Fig. 3; P \ 0.05). P. rubicunda
was found to have significantly greater masseter leverages at the incisor and canine than the other four species (P \ 0.001). Masseter leverages of T. phayrei at the
incisor and canine were significantly greater than those
of S. vetulus and T. obscurus (P \ 0.01), but these leverages were not significantly different from those of P.
comata. The mechanical advantages for the medial pterygoid at P3 and M1 were significantly greater in P. rubicunda and T. phayrei compared to P. comata, S. vetulus,
and T. obscurus (Fig. 4; P \ 0.05). The medial pterygoid
leverages of P. rubicunda at the incisor and canine were
significantly greater than those of P. comata, S. vetulus,
T. phayrei, and T. obscurus (P \ 0.01). T. phayrei showed
significantly greater medial pterygoid leverage at the incisor compared to P. comata, S. vetulus, and T. obscurus
(P \ 0.05). The mechanical advantage for the medial
pterygoid of T. phayrei at the canine was significantly
greater than that of S. vetulus and T. obscurus (P \
0.01), but it was not significantly different from that of
P. comata. No significant difference was found between
species for the temporalis leverages at any bite point
(see Fig. 5). P. rubicunda and T. phayrei exhibited more
medially positioned M1s relative to the biarticular
breadth than the other three colobines (Table 3; P \
0.05).
The relative positions of the masseter were significantly different between seed eaters and non-seed eaters
(Table 3; P \ 0.05). P. rubicunda had relatively more
anteriorly positioned medial pterygoid than S. vetulus
and T. phayrei (P \ 0.05). The relative position of the
temporalis was not significantly different between species. The biarticular breadth of P. rubicunda was significantly wider than that of T. obscurus and T. phayrei
(P \ 0.05). P. comata appeared to possess significantly
American Journal of Physical Anthropology
142
D.B. KOYABU AND H. ENDO
Fig. 3. Plot comparing the mechanical advantages of the masseter muscle at the incisor, canine, P3, and M1. The box represents
the interquartile range, the horizontal bar encloses the central 90% of the data, and the vertical bar indicates the median.
Fig. 4. Plot comparing the mechanical advantages of the medial pterygoid muscle at the incisor, canine, P3, and M1. The box
represents the interquartile range, the horizontal bar encloses the central 90% of the data, and the vertical bar indicates the
median.
wider bilateral breadth of M1 than the other four species
(P \ 0.05). Molar row lengths were significantly shorter
in P. rubicunda and T. phayrei compared to the other
three colobine species (P \ 0.05).
DISCUSSION
Craniodental arrangements and
mechanical advantage
Both of the seed eaters, P. rubicunda and T. phayrei,
exhibit relatively greater mechanical advantage of the
masseter and medial pterygoid muscles at P3 and M1
(Table 3; Figs. 3 and 4) compared to P. comata, T. obscurus, and S. vetulus. This finding is concordant with our
prediction that seed predators should exhibit greater
masticatory leverage at more posterior bite points. In
contrast, the temporalis leverage along the postcanine
tooth row is comparable between the seed eaters and
species that rarely feed on seeds. Therefore, while the
leverages for the masseter and medial pterygoid muscles
American Journal of Physical Anthropology
along the postcanine tooth row are markedly increased
in seed eaters, it appears that the temporalis leverage is
relatively conserved among the five species studied. The
increased leverage of the masseter and medial pterygoid
muscles along the postcanine tooth row in the seed eaters may provide advantages for feeding on resistant
seeds, as greater bite forces can be produced at a given
muscle force. In various primates, species that feed on
resistant foods are often found to possess craniodental
features adapted for forceful biting (Bouvier, 1986a,b;
Demes and Creel, 1988; Ravosa, 1990; Antón, 1996;
Spencer, 1999, 2003; Taylor, 2002, 2006a,b; Vinyard
et al., 2003; Singleton, 2004, 2005; Wright, 2005). The
craniodental morphology of the seed-eating African colobines exhibits a greater mechanical advantage of the
masseter at the molar than that of the young-leaf-eating
colobines, indicating that the seed eaters can generate
greater bite forces at a given muscle force (Koyabu and
Endo, 2009). Wright (2005) found that Cebus apella,
which feeds on markedly tough food items, exhibits
greater mechanical advantage of the masseter and tem-
CRANIODENTAL MECHANICS IN ASIAN COLOBINES
143
Fig. 5. Plot comparing the mechanical advantages of the temporalis muscle at the incisor, canine, P3, and M1. The box represents the interquartile range, the horizontal bar encloses the central 90% of the data, and the vertical bar indicates the median.
poralis muscles compared to C. olivaceus. However, the
leverage of the medial pterygoid was found to be comparable, leading him to suggest that its anterior migration
is impeded by the position of the third molars (Wright,
2005). In contrast, the increased leverage of the medial
pterygoid muscle and reduction in the molar row length
found in the seed-eating leaf monkeys implies that dental reduction may have allowed the anterior migration of
the medial pterygoid muscle. The finding that the temporalis leverage along the postcanine tooth row is comparable between species runs somewhat counter to our
prediction. Given that mammals that depend on their
anterior dentition (e.g., carnivores) possess relatively
larger temporalis muscle (Turnbull, 1970; Moore, 1981),
it is possible that physiological cross-sectional area of
the temporalis may vary between the seed eaters and
species that rarely feed on seeds.
P. rubicunda and T. phayrei are also characterized by
more medially positioned tooth rows relative to biarticular breadth than the other three colobines (Table 3). In
African colobines, the seed eaters similarly possess more
medially positioned tooth rows compared to species that
rarely predate seeds (Koyabu and Endo, 2009). Under
the constrained lever model, postcanine dental batteries
closer to the sagittal plane allow a greater amount of
available balancing-side muscle force to be converted to
bite force without producing distractive forces at the
TMJ (Hylander, 1977; Spencer, 1999). Therefore, with
more medially positioned tooth rows and greater mechanical advantage along the postcanine tooth row, P.
rubicunda and T. phayrei may be capable of generating
greater bite forces during chewing without provoking
TMJ distraction compared to P. comata, T. obscurus, and
S. vetulus.
In accordance with our prediction, the sclerocarpic forager P. rubicunda exhibited increased masticatory leverage at the anterior dental bite points. P. rubicunda
exhibits greater masseter and medial pterygoid leverages at the anterior dentition than P. comata, S. vetulus,
and T. obscurus. T. phayrei exhibits significantly greater
masseter and medial pterygoid leverages at the anterior
dentition than S. vetulus and T. obscurus, but those leverages are not significantly different from P. comata (Table 3; Figs. 3 and 4). When leverage at the anterior den-
tition is compared between the seed eaters, the leverages
for the masseter and medial pterygoid muscles in
P. rubicunda are significantly greater than those in
T. phayrei. Thus, P. rubicunda may be capable of efficiently generating greater bite forces at both the anterior
and postcanine dentition, whereas the craniodental
arrangement in T. phayrei may be less specialized for
forceful incision.
It is possible that the difference in muscle leverage at
the anterior dentition between P. rubicunda and
T. phayrei is associated with exploitation of immature
seeds. P. rubicunda feeds on mature seeds, but was also
seen frequently feeding on immature seeds from unripe
fruits in Sepilok, Northern Borneo (Davies, 1991). In the
case of fruits such as Xerospermum internedium, Wallucharia wallichii, and Knema laterica, their resistant
arils are scraped off and removed to access the seeds
(Davies, 1991). In addition, P. rubicunda was reported to
forage on seeds of unripe Litsea fruits, occasionally discarding the pericarps and mesocarps. Seeds were shown
to be predated extensively by T. phayrei in both Gumti
and Phu Khieo (Gupta and Kumar, 1994; Suarez, 2006),
but these seeds were rarely collected from unripe fleshy
fruits (Gupta and Kumar, 1994; Suarez, 2006), in contrast to the behavior of P. rubicunda.
As noted earlier, Chiropotes predates on immature
seeds from unripe fruits, which have pericarps of higher
puncture resistance, whereas Pithecia feeds more frequently on ripe seeds, which are not protected by resistant pericarps (Kinzey and Norconk, 1993). Compared
with Pithecia, Chiropotes has a larger canine root surface area, which was suggested to be related to its distinctive sclerocarpic harvesting behavior (Spencer, 2003).
As illustrated by Chiropotes and Pithecia, seed choice
and the manner of feeding involved in seed eating may
differ among the seed-eating Asian colobines. The
remarkably greater masticatory leverage at the anterior
dentition in P. rubicunda may be related to its sclerocarpic harvesting and forceful incision. Conversely, the
lack of high masticatory leverage at the anterior dentition in T. phayrei suggests that biting into unripe fleshy
fruits with its anterior dentition is relatively unimportant in this species. Instead, the increased masticatory
leverage along the postcanine tooth row in T. phayrei
American Journal of Physical Anthropology
American Journal of Physical Anthropology
*
*
*
0.050
0.051
0.076
0.130
**
0.916
***
**
***
0.309
0.723
0.604
0.283
***
***
0.056
**
**
0.118
0.062
0.746
0.709
0.438
0.862
0.621
0.731
0.815
0.775
*
0.062
0.808
**
*
0.733
0.525
0.098
*
**
***
0.468
0.328
*
*
*
0.151
**
*
0.897
0.859
0.897
0.965
***
***
***
***
***
***
0.664
0.070
0.188
***
***
***
***
***
***
***
***
***
***
0.244
0.254
0.536
0.536
**
***
***
***
***
**
0.311
*
0.109
***
***
***
***
***
***
***
***
***
***
0.199
0.110
0.627
0.186
0.756
***
0.085
***
0.336
0.767
0.134
*
0.244
***
0.133
***
***
0.059
**
*
**
0.890
0.091
0.138
0.093
0.312
0.172
0.051
0.801
0.420
0.730
0.696
*
0.982
0.909
0.801
0.982
0.267
0.986
0.925
0.845
0.309
*
*
*
0.080
0.641
0.604
0.866
0.899
a
* Significant at P \ 0.05; ** significant at P \ 0.01; *** significant at P \ 0.001.
Pairwise comparisons are based on Mann–Whitney U test.
b
Mechanical advantages are computed as the ratio of the muscle position and the load arm for biting (Demes and Creel, 1988; Koyabu and Endo, 2009).
0.755
0.345
0.950
0.228
*
*
0.694
*
*
0.305
0.340
0.227
*
0.536
0.227
0.840
0.768
0.840
0.904
**
0.602
0.968
0.547
*
*
***
versus Biarticular breadth
Bilateral M1 breadth
versus Geometric mean
Masseter position
Medial pterygoid position
Temporalis position
Biarticular breadth
Bilateral M1 breadth
Incisor—articular eminence
distance
Canine—articular eminence
distance
P3—articular eminence
distance
M1—articular eminence
distance
Molar row length
***
***
***
***
***
***
***
***
0.297
0.574
0.297
0.570
Mechanical advantageb
Masseter/incisor
Masseter/canine
Masseter/P3
Masseter/M1
Medial pterygoid/incisor
Medial pterygoid/canine
Medial pterygoid/P3
Medial pterygoid/M1
Temporalis/incisor
Temporalis/canine
Temporalis/P3
Temporalis/M1
***
0.492
0.091
0.717
**
*
0.351
0.968
0.657
0.717
*
**
**
***
***
***
***
***
***
0.605
0.853
0.705
0.468
*
0.191
0.058
0.895
*
0.105
0.166
0.985
0.836
0.611
*
***
**
***
***
***
**
***
***
0.138
0.179
0.195
0.164
P. comata
P. comata vs
P. comata
P. comata
P. rubicunda P. rubicunda P. rubicunda S. vetulus vs S. vetulus
T. obscurus
vs P. rubicunda S. vetulus vs T. obscurus vs T. phayrei vs S. vetulus vs T. obscurus vs T. phayrei T. obscurus vs T. phayrei vs T. phayrei
TABLE 4. Significance tests for differences in mechanical advantages and shape ratiosa
144
D.B. KOYABU AND H. ENDO
CRANIODENTAL MECHANICS IN ASIAN COLOBINES
suggests that it relies more on forceful mastication and
processes mature seeds mainly with the postcanine dentition. However, our postulation is not yet clear because
detailed behavioral data are lacking on the relative
amounts of seed processing that take place at the anterior versus posterior dentition in colobine monkeys.
Because incision and mastication produce contrasting
stress patterns in the dentition and mandibles
(Hylander, 1988, Spencer, 2003), morphological studies
on teeth and jaw form are needed in addition to field
studies to test whether differences exist in the preferential use of anterior dentition versus postcanine dentition
among colobines [but see Daegling and McGraw (2007)].
Dental proportions
Molar rows are significantly shorter in the seed-eating
P. rubicunda and T. phayrei compared to the other three
colobines (Table 3). The functional significance of the
molar row reduction found in the seed predators here
may be explained by the constrained lever model [see
Greaves (1978), Spencer and Demes (1993) and Spencer
(1999)]. This model suggests that craniodental arrangements of anthropoid primates are constrained by the
trade-off between increasing bite force magnitudes and
avoiding TMJ distractions (Spencer, 1999). Precontact
Inuit, whose traditional diet required frequent forceful
biting, exhibits a more posteriorly positioned dentition
and more anteriorly positioned masseter and temporalis
muscles, compared to behaviorally unspecialized populations (Spencer and Demes, 1993). It has been suggested
that the third molar agenesis found in the precontact
Inuit, a configurational change that would keep the muscle resultant force enclosed within the triangle of support defined by the TMJs and bite point, was selected to
minimize the occurrence of this distraction (Spencer and
Demes, 1993). Reduction of molar occlusal areas found
in New World monkeys specialized for forceful biting,
particularly Cacajao (Rosenberger, 1992) and Cebus
(Wright, 2005), may be a comparable consequence of preventing the distal molars from being pushed into the
posterior region of the mandible (Spencer, 1999; Wright,
2005). The seed-eating African colobines, which possess
greater mechanical advantage for the masseter, also exhibit relatively shorter postcanine tooth rows compared
to colobines that eat young leaves (Koyabu and Endo,
2009).
Similarly in P. rubicunda and T. phayrei, it is possible
that the anterior migration of the masticatory muscle
has favored a concomitant reduction of the molar row
(Table 3). It may be that, while anterior migration of
masticatory muscles enabled increased leverage for biting in seed eaters by positioning the midline muscle resultant force more anteriorly, reduction of the posterior
region of the molars has been coselected to keep the dentition in safe spatial arrangements in the masticatory
apparatus and prevent the muscle resultant force from
falling outside the triangle of support.
Seed eating in colobine monkeys
Seed eating in P. rubicunda and T. phayrei. As
noted earlier, although young leaves are generally preferred by P. rubicunda in Sepilok Forest, seeds are also
extensively foraged throughout the year and comprise
more than 80% of the diet in certain seasons (Davies,
145
1991). In Gumti, 23% of the annual diet of T. phayrei is
seeds, and seed consumption reaches more than 70% of
the diet in March, which coincides with the period of
least abundance of young leaves (Gupta and Kumar,
1994). P. rubicunda feeds on the seeds of Millettia (Davies, 1991), which require a force of 167 N for fracture
(Lambert et al., 2004). Millettia seeds are noted as particularly stress-limited foods that are not predated by
Cercopithecus ascanius in Uganda, but are foraged by
the sympatric Lophocebus albigena (Lambert et al.,
2004), which possesses a masticatory configuration with
increased biting leverage (Singleton, 2005). Although we
lack detailed data on the strength of the foods consumed
by T. phayrei, the seeds most frequently foraged in
Gumti are those of Albizzia (Gupta and Kumar, 1994),
the seed shells of which are reported to have a hardness
(resistance to indentation) of 267 MPa (Lucas, 2004a).
This is even harder than Macadamia nut shells (180
MPa) (Lucas, 2004a), which are often noted as a typical
stress-limited food (Lucas et al., 1994, 2008; Taylor,
2006b). Because falling back on resistant foods in certain
seasons may pose selective pressures on primates (Lambert, 2007; Marshall and Wrangham, 2007), craniodental
features found in P. rubicunda and T. phayrei, such as
greater mechanical advantage for mastication, medially
positioned tooth rows, and shorter postcanine teeth, may
have evolved for generating greater bite forces and processing stress-limited seeds.
Seed eating in the subfamily Colobinae. Ecological
studies have revealed that seed eating is a major feature of colobine diet in both Africa (Maisels et al.,
1994; Oates, 1994; Davies et al., 1999) and Asia (Davies et al., 1988; Davies, 1991; Bennett and Davies,
1994). In terms of dental morphology, Teaford (1983b)
found that the seed-eating P. rubicunda is equipped
with relatively shorter shearing crests than the more
folivorous T. cristatus. Among African colobines, C.
satanas, which is a selective seed eater (McKey, 1978;
McKey et al., 1981; Oates, 1994), is reported to have
relatively flatter molars compared to the more folivorous C. guereza and P. badius (Kay, 1984; Ungar,
1998). In general, while highly crested teeth are well
suited for processing displacement-limited items such
as leaves, rounder and flatter cusped teeth are effective for fracturing stress-limited foods such as seeds
(Lucas, 2004a). Adding to the fact that dental shape
variation in colobines may be related to seed predation, advantageous arrangements and greater mechanical efficiency of the masticatory apparatus found in
seed-eating Asian colobines (this study) and African
colobines (Koyabu and Endo, 2009) suggest that certain seed-eating colobine species are capable of generating greater bite forces and feeding on stress-limited
food items. Seeds are more difficult to process compared to other relatively soft foods (e.g., pulpy ripe
fruits) and require relatively stronger masticatory force
to break down (Lucas and Teaford, 1994; Lucas et al.,
2000); however, seed eating may be an important aspect of the colobine diet, given that seeds are a rich
source of nutrition (Lucas and Teaford, 1994; Maisels
et al., 1994; Waterman and Kool, 1994; Norconk et al.,
1998). In the case of Colobus satanas from Cameroon,
it has been pointed out that seeds are predated for
their high concentrations of lipids and digestible carbohydrates (McKey, 1978). Albizzia lebbek seeds, which
are predated extensively by T. phayrei, have a high
American Journal of Physical Anthropology
146
D.B. KOYABU AND H. ENDO
protein concentration (38% of dry weight) and some
lipids (6%; Auta and Anwa, 2007). Davies et al. (1988)
similarly reported that the seeds selected by P. rubicunda have, on average, high concentrations of lipids
and fair levels of protein. As Kinzey (1992) has suggested, seeds may be a nutritionally desirable food for
primates, owing to the high lipid and/or protein content of seeds, as long as the stress-limited defense of
the seeds can be overcome.
Furthermore, as noted above, the differences in mechanical advantages for incision between P. rubicunda
and T. phayrei should be taken into consideration. Kinzey (1992) noted that seeds in the early stages of development are less stress-limited than mature seeds,
but are still protected by the resistant unripe pericarp.
Immature seeds, which have higher nutritional value
and less toxic secondary compounds than mature
seeds, may be desirable food items for primates that
are able to husk the resistant pericarp with their anterior dentition and gain access to the immature seeds
(Kinzey, 1992). Given that P. rubicunda feeds frequently on seeds from unripe fleshy fruits (Davies,
1991), the marked mechanical advantages at the anterior dentition in P. rubicunda may be related to sclerocarpic harvesting.
Although our study supports craniodental divergence
between the seed predators and species that rarely feed
on seeds, detailed comparative studies on the mechanical
properties of foods consumed by the Asian colobines and
the feeding behaviors of these colobine species are
needed to confirm our findings. In addition, as the physiological cross-sectional area of the masticatory muscle is
also an important contributor to the maximum bite force
an animal can generate (Raadsheer, 1999), future studies on physiological cross-sectional area of masticatory
muscles would provide valuable perspectives illuminating the craniofacial adaptation of colobines.
CONCLUSIONS
The results of this study highlight the distinctive craniodental divergence among the colobine monkeys,
potentially related to seed predation. Seed-eating Asian
colobines (P. rubicunda and T. phayrei) exhibit greater
leverage of the masseter and medial pterygoid muscles
for mastication and more medially positioned tooth rows
compared to the colobines, which rarely exploit seeds (P.
comata, T. obscurus, and S. vetulus). These morphological patterns indicate that seed-eating colobines are
equipped with a more mechanically efficient masticatory
structure for postcanine chewing and are capable of generating stronger occlusal loads at a given muscle force.
The masseter and medial pterygoid muscle leverages for
incision are found to be increased in P. rubicunda, but
those of T. phayrei are not significantly different from
that of P. comata. This may suggest that P. rubicunda is
well adapted to biting at both posterior and anterior dental bite points, whereas T. phayrei depends more on
forceful mastication and does not require frequent incision or canine use. The seed eaters are also characterized by a significantly reduced molar row. As greater
bite force may potentially provoke injurious distractive
forces at the balancing-side TMJ, the molar reduction
found in the seed eaters may have been selected together
with increased biting leverage to prevent the distal
molars from being pushed into the posterior region of
the mandible and to keep the midline muscle resultant
force enclosed within the triangle of support. Our findings suggest that mature and/or immature seed foraging
may have been a selective agent responsible for the craniodental variation we find among some Asian colobines.
This study points out the significance of seed predation
for the evolution of colobine skull morphology.
ACKNOWLEDGMENTS
We are grateful to N. Egi, Y. Hamada, H. Ihobe, Y.
Kunimatsu, T. Mouri, M. Nakatsukasa, T. Nishimura,
M. Oishi, D. Shimizu, G. Suwa, and M. Takai for suggestions and helpful comments on the work. We also greatly
appreciate two anonymous reviewers for improving the
quality of this article. The authors thank S. Kawada of
National Science Museum, Tokyo; P. Jenkins, L. Tomsett,
and D. Hills of British Museum of Natural History; K.
Lim of Raffles Museum of Biodiversity Research,
National University of Singapore; for their kind help
during examinations of specimens.
APPENDIX
TABLE A1. Studied specimens
Species
Storage
Specimen Examined
P. comata
BMNH
ZRC
NSMT
BMNH
ZRC
BMNH
44-3-20-10, 54-54, 1845-4-2-4, 54-55, 54-52, 1850-8-15-4
4-223, 4-228, 4-227
9505
94-6-12-12, 55-728, 92-11-28-1, 1908-7-17-2, 1842-1-19-93
4-347, 4-356, 4-360, 4-364, 4-365
11-9-9-1, 15-3-1-5, 23-1-18-2, 23-1-18-3, 66-5544, 79-9-5-2, 1923-1-19-1,
1928-7-12-1, 1950-7-17-6, 1950-7-17-7, 1975-1806, 1975-1807
14-12-8-27, 55-1534, 55-1535, 55-154, 71-722, 71-749
4-448, 4-450, 4-455, 4-460, 4-485,
4-487, 4-495, 4-500, 4-501, 4-511, 4-522, 4-529
14-7-19-3, 14-7-8-1, 14-7-8-2, 15-12-1-2, 15-12-1-5, 15-5-5-9, 17-4-24-1,
24-9-2-10, 24-9-2-11, 36-12-26-1, 1914-8-22-7, 1924-9-2-9, 1937-9-10-12,
1937-9-10-4, 1937-9-10-6, 1937-9-10-7
P. rubicunda
S. vetulus
T. obscurus
BMNH
ZRC
T. phayrei
BMNH
BMNH, British Museum of Natural History; NSMT, National Science Museum, Tokyo; ZRC, Zoological Reference Collection,
National University of Singapore.
American Journal of Physical Anthropology
CRANIODENTAL MECHANICS IN ASIAN COLOBINES
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