Craniodental mechanics and diet in Asian colobines Morphological evidence of mature seed predation and sclerocarpy.код для вставкиСкачать
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: email@example.com 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 LITERATURE CITED Antón SC. 1996. Cranial adaptation to a high attrition diet in Japanese macaques. Int J Primatol 17:401–427. Auta J, Anwa EP. 2007. Preliminary studies on Albizzia lebbeck seeds: proximate analysis and phytochemical screening. Res J Biol Sci 2:33–35. Ayres JM. 1986. Uakaris and Amazonian ﬂooded forest. Ph.D. Dissertation, University of Cambridge. Ayres JM. 1989. Comparative feeding ecology of the uakari and bearded saki, Cacajao and Chiropotes. J Hum Evol 18:697– 716. Bennett EL, Davies AG. 1994. The ecology of Asian colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p 129–171. Bouvier M. 1986a. A biomechanical analysis of mandibular scaling in Old World monkeys. Am J Phys Anthropol 69:473– 482. Bouvier M. 1986b. Biomechanical scaling of mandibular dimensions in New World monkeys. Int J Primatol 7:551–567. Chapman CA, Chapman LJ, Gillespie TR. 2002. Scale issues in the study of primate foraging: red colobus of Kibale National Park. Am J Phys Anthropol 117:349–363. Curtin SH. 1976. Niche separation in sympatric Malaysian leafmonkeys (Presbytis obscura and Presbytis melalophos). Yearb Phys Anthropol 20:421–439. Daegling DJ, McGraw WS. 2001. Feeding, diet, and jaw form in West African Colobus and Procolobus. Int J Primatol 22:1033–1055. Daegling DJ, McGraw WS. 2007. Functional morphology of the mangabey mandibular corpus: relationship to dental specializations and feeding behavior. Am J Phys Anthropol 134:50– 62. Darroch JN, Mosimann JE. 1985. Canonical and principal components of shape. Biometrika 72:241–252. Dasilva GL. 1994. Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. Int J Primatol 15:655–680. Davies AG. 1991. Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of Northern Borneo. Int J Primatol 12:119–144. Davies AG, Bennett EL, Waterman PG. 1988. Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biol J Linn Soc 34:33–56. Davies AG, Oates JF, Dasilva GL. 1999. Patterns of frugivory in three West African colobine monkeys. Int J Primatol 20:327– 357. Dela JDS. 2007. Seasonal food use strategies of Semnopithecus vetulus nestor, at Panadura and Piliyandala, Sri Lanka. Int J Primatol 28:607–626. Demes B, Creel N. 1988. Bite force, diet, and cranial morphology of fossil hominids. J Hum Evol 17:657–670. Du Brul EL. 1977. Early hominid feeding mechanisms. Am J Phys Anthropol 47:305–320. Greaves WS. 1978. The jaw lever system in ungulates: a new model. J Zool 184:271–285. Gupta AK, Kumar A. 1994. Feeding ecology and conservation of the Phayre’s leaf monkey Presbytis phayrei in northeast India. Biol Conserv 69:301–306. Hayes VJ, Freedman L, Oxnard CE. 1996. Dental sexual dimorphism and morphology in African colobus monkeys as related to diet. Int J Primatol 17:725–757. Herring SW. 1993. Functional morphology of mammalian mastication. Am Zool 33:289. Hladik CM. 1977. A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In: Clutton-Brock TH, editor. Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. London: Academic Press. p 323–353. Hull DB. 1979. A craniometric study of the black and white Colobus Illiger 1811 (Primates: Ceropithecoidea). Am J Phys Anthropol 51:163–181. 147 Hylander WL. 1975. Incisor size and diet in anthropoids with special reference to Cercopithecidae. Science 189:1095–1098. Hylander WL. 1977. The adaptive signiﬁcance of Eskimo craniofacial morphology. In: Dahlberg AA, Graber TM, editors. Orofacial growth and development. Paris: Mouton. p 129–170. Hylander WL. 1979. The functional signiﬁcance of primate mandibular form. J Morphol 160:223–239. Hylander WL. 1988. Implications of in vivo experiments for interpreting the functional signiﬁcance of ‘‘robust’’ australopithecine jaws. In: Grine FE, editor. Evolutionary history of the ‘‘robust’’ australopithecines. New York: Aldine de Gruyter. p 55–83. Jablonski NG, Pan RL, Chaplin G. 1998. Mandibular morphology of the doucs and snub-nosed monkeys in relation to diet. In: Jablonski NG, editor. The natural history of the doucs and snub-nosed monkeys. Singapore: World Scientiﬁc. p 105–128. Jungers WL, Falsetti AB, Wall CE. 1995. Shape, relative size, and size-adjustments in morphometrics. Yearb Phys Anthropol 38:137–161. Kay RF. 1984. On the use of anatomical features to infer foraging behavior in extinct primates. In: Rodman PS, Cant JGH, editors. Adaptations for foraging in nonhuman primates: contributions to an organismal biology of prosimians, monkeys and apes. New York: Columbia University Press. p 21–53. Kinzey WG. 1992. Dietary and dental adaptations in the Pitheciinae. Am J Phys Anthropol 88:499–514. Kinzey WG, Norconk MA. 1990. Hardness as a basis of fruit choice in two sympatric primates. Am J Phys Anthropol 81:5– 15. Kinzey WG, Norconk MA. 1993. Physical and chemical properties of fruit and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. Int J Primatol 14:207–227. Koyabu DB, Endo H. 2009. Craniofacial variation and dietary adaptations of African colobines. J Hum Evol 56:525–536. Lambert JE. 2007. Seasonally, fallback strategies, and natural selection. In: Ungar PS, editor. Evolution of the human diet: the known, the unknown, and the unknowable. New York: Oxford University Press. p 324–343. Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125:363–368. Leutenegger W. 1971. Metric variability of the postcanine dentition in colobus monkeys. Am J Phys Anthropol 35:91–100. Lucas PW. 2004a. Dental functional morphology: how teeth work. Cambridge: Cambridge University Press. Lucas PW. 2004b. Plant mechanics and primate dental adaptations: an overview. In: Anapol F, German RZ, Jablonski NG, editors. Shaping primate evolution: form, function, and behavior. New York: Cambridge University Press. p 193–205. Lucas PW, Constantino P, Wood BA, Lawn B. 2008. Dental enamel as a dietary indicator in mammals. Bioessays 30:374– 385. Lucas PW, Peters CR. 2000. Function of postcanine tooth crown shape in mammals. In: Teaford MF, Smith MM, Ferguson MWJ, editors. Development, function and evolution of teeth. New York: Cambridge University Press. p 282–289. Lucas PW, Peters CR, Arrandale SR. 1994. Seed-breaking forces exerted by orang-utans with their teeth in captivity and a new technique for estimating forces produced in the wild. Am J Phys Anthropol 94:365–378. Lucas PW, Prinz JF, Agrawal KR, Bruce IC. 2002. Food physics and oral physiology. Food Qual Prefer 13:203–213. Lucas PW, Teaford MF. 1994. Functional morphology of colobine teeth. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behavior and evolution. Cambridge: Cambridge University Press. p 173–203. Lucas PW, Turner IM, Dominy NJ, Yamashita N. 2000. Mechanical defences to herbivory. Ann Bot 86:913–920. Maisels F, Gautier-Hion A, Gautier JP. 1994. Diets of two sympatric colobines in Zaire: more evidence on seed-eating in forests on poor soils. Int J Primatol 15:681–701. Marshall AJ, Wrangham RW. 2007. Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235. American Journal of Physical Anthropology 148 D.B. KOYABU AND H. ENDO Martin R, Knussmann R. 1988. Anthropologie. Stuttgart: Gustav Fischer. McKey DB. 1978. Soils, vegetation, and seed-eating by black colobus monkeys. The ecology of arboreal folivores. Washington DC: Smithsonian Institution Press. p 423–437. McKey DB, Gartlan JS, Waterman PG, Choo GM. 1981. Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry. Biol J Linn Soc 16:115–146. Moore WJ. 1981. The mammalian skull. Cambridge: Cambridge University Press. Norconk MA, Grafton BW, Conklin-Brittain NL. 1998. Seed dispersal by neotropical seed predators. Am J Primatol 45:103– 126. Oates JF. 1977. The guereza and its food. In: Clutton-Brock TH, editor. Primate ecology. London: Academic Press. p 276–321. Oates JF. 1994. The natural history of African colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p 75–128. Oates JF, Davies AG. 1994. What are the colobines. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p 1–10. O’Higgins P, Pan RL. 2004. Facial growth and phylogeny of the African colobines. In: Anapol F, German RZ, Jablonski N, editors. Shaping primate evolution; form, function and behavior. Cambridge: Cambridge University Press. p 24–44. Osborn JW. 1987. Relationship between the mandibular condyle and the occlusal plane during hominid evolution: some of its effects on jaw mechanics. Am J Phys Anthropol 73:193–207. Pan RL. 2006. Dental morphometric variation between African and Asian colobines, with special reference to the other Old World monkeys. J Morphol 267:1087–1098. Pan RL, Groves CP. 2004. Cranial variation among the Asian colobines. In: Anapol F, German RZ, Jablonski N, editors. Shaping primate evolution; form, function and behavior. Cambridge: Cambridge University Press. p 45–65. Pan RL, Peng Y, Ye Z, Wang H, Yu F. 1995. Comparison of masticatory morphology between Rhinopithecus bieti and R. roxellana. Am J Primatol 35:271–281. Raadsheer MC. 1999. Contribution of jaw muscle size and craniofacial morphology to human bite force magnitude. J Dent Res 78:31–42. Radinsky L. 1985. Patterns in the evolution of ungulate jaw shape. Am Zool 25:303. Ravosa MJ. 1990. Functional assessment of subfamily variation in maxillomandibular morphology among Old World monkeys. Am J Phys Anthropol 82:199–212. Ravosa MJ. 1996. Jaw morphology and function in living and fossil Old World monkeys. Int J Primatol 17:909–932. Rosenberger AL. 1992. Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–562. Ruhiyat Y. 1983. Socio-ecological study of Presbytis aygula in West Java. Primates 24:344–359. Schultz AH. 1958. Cranial and dental variability in colobus monkeys. Proc Zool Soc Lond 130:79–105. Singleton M. 2004. Geometric morphometric analysis of functional divergence in mangabey facial form. J Anthropol Sci 82:27–44. American Journal of Physical Anthropology Singleton M. 2005. Functional shape variation in the Cercopithecine masticatory complex. In: Slice DE, editor. Modern morphometrics in physical anthropology. New York: Kluwer. p 319–348. Spencer MA. 1998. Force production in the primate masticatory system: electromyographic tests of biomechanical hypotheses. J Hum Evol 34:25–54. Spencer MA. 1999. Constraints on masticatory system evolution in anthropoid primates. Am J Phys Anthropol 108:483–506. Spencer MA. 2003. Tooth-root form and function in platyrrhine seed-eaters. Am J Phys Anthropol 122:325–335. Spencer MA, Demes B. 1993. Biomechanical analysis of masticatory system conﬁguration in Neandertals and Inuits. Am J Phys Anthropol 91:1–20. Struhsaker TT. 1975. The red colobus monkey. Chicago: University of Chicago Press. Suarez SA. 2006. Phayre’s leaf monkeys (Trachypithecys phayrei) as seed predators in the Phu Khieo Wildlife Sanctuary, Thailand. Am J Phys Anthropol Suppl 129:173. Swindler DR, Orlosky FJ. 1974. Metric and morphological variability in the dentition of colobine monkeys. J Hum Evol 3:135–160. Taylor AB. 2002. Masticatory form and function in the African apes. Am J Phys Anthropol 117:133–156. Taylor AB. 2006a. Diet and mandibular morphology in African apes. Int J Primatol 27:181–201. Taylor AB. 2006b. Feeding behavior, diet, and the functional consequences of jaw form in orangutans, with implications for the evolution of Pongo. J Hum Evol 50:377–393. Teaford MF. 1983a. Functional morphology of the underbite in two species of langurs. J Dent Res 62:183. Teaford MF. 1983b. The morphology and wear of the lingual notch in macaques and langurs. Am J Phys Anthropol 60:7– 14. Teaford MF, Ungar PS. 2000. Diet and the evolution of the earliest human ancestors. Proc Natl Acad Sci USA 97:13506– 13511. Turnbull WD. 1970. Mammalian masticatory apparatus. Fieldiana Geol 18:153–356. Ungar P. 1998. Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evol Anthropol 6:205–217. van Roosmalen MGM, Mittermeier RA, Fleagle JG. 1988. Diet of the northern bearded saki (Chiropotes satanas chiropotes): a neotropical seed predator. Am J Primatol 14:11–35. Verheyen WN. 1962. Contribution à la craniologie comparée des primates. Musee R Afr Cent 105:1–211. Vinyard CJ, Wall CE, Williams SH, Hylander WL. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120:153–170. Waterman PG, Kool KM. 1994. Colobine food selection and plant chemistry. In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge: Cambridge University Press. p 251–284. Willis MS, Swindler DR. 2004. Molar size and shape variations among Asian colobines. Am J Phys Anthropol 125:51–60. Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48:473–492. Yeager CP. 1989. Feeding ecology of the proboscis monkey (Nasalis larvatus). Int J Primatol 10:497–530.