zy zyxwvutsr zyxwvu zyxwvu zyxwvuts zyx zyxwvu AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 94:239-261 (1994) Morphological Adaptation to Diet in Platyrrhine Primates FRED ANAPOL AND SARAH LEE Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53201 (FA.); Department of Human Anatomy and Cell Biology, The University of Liuerpool, Liuerpool L69 3BX, UK (S.L.) KEY WORDS New World monkeys morphology, Mandible teeth mastication Protein functional ABSTRACT Morphological features of the jaws and teeth are examined in eight species of platyrrhine monkeys that coexist in the Suriname rainforest. Z-scores calculated from geometric predictions for several features of the feeding apparatus thought to have some functional significance (e.g., tooth dimensions, jaw robusticity, leverage of primary jaw elevators) are compared to a profile of the naturalistic dietary behavior of these species (i.e., proportions of fruit mesocarp, seeds, leaves, and fauna eaten). Several features are found exclusively in those platyrrhines whose dietary preferences are the most limited. Such specializations appear to be associated with a particular protein source exploited by a species to supplement a largely frugivorous diet. Ateles paniscus, which feeds primarily on the mesocarp of ripe fruit, has an adaptive morphology that emphasizes broad incisors. Chiropotes satanas (and to a slightly lesser extent, Pithecia pithecia) is a frugivorel seed predator with large upper and lower canines and a robust mandible. The frugivorelfolivore Alouatta seniculus has a relatively large total molar area and effective mandibular condyle height. In all four of these strictly vegetarian species, the leverage of the masseter muscle is greater than that of temporalis. Of the omnivorous species, Cebus apella and C. nigrivittatus exploit both fauna and seeds for protein and exhibit an array of many of the above features, such as large teeth and thick mandibles. Saimiri sciureus, not particularly known for seed predation, departs from Cebus in having less robust canines and a more gracile mandible. All three cebid omnivores have a temporalis with greater leverage than the masseter, indicating a requirement €or resisting anteriorly directed forces, €or example, using the jaws for vigorous foraging. The lack of any enlarged features, other than incisors, in the omnivorous Saguinus midas may be attributable to the functional constraints of small body size. Because the small size of the gape limits the size of the food parcel ingested, a requirement to enlarge other dentomandibular structures for trituration is alleviated. o 1994 Wiley-Liss, Inc. Structure-function relationships are of particular interest to evolutionary morphologists concerned with the adaptation of individual species to particular behavioral niches. Furthermore, because the fossil record consists largely of remnants of individuals whose activitycannotbe observed inferences about paleobehavior must be extrapolated from studies of extant 0 1994 WILEY-LISS. INC. creatures whose behavioral modes are known: The close link between structure and function of jaws and teeth in living zy zyxw Recieved October 29,1990; accepted February 1,1994. Address reprint requests t o Fred Anapol, Department of Anthropology, University of Wisconsin-Milwaukee, Bolton Hall, P.O. B~~ 413, Milwaukee, WI53201. 240 zyxwvut zyxwv zyxwvut zyxwvutsrq F. ANAPOL AND S. LEE forms allows paleofeeding behavior to be in- to triturate foods ordinarily consumed by terpreted by analogy (e.g., Cachel, 1983; primates in the wild (e.g., I(lnzey and NorKay and Covert, 1984; Ravosa, 1991). Such conk, 1990). The goal of this study is to partition a interpretations, however, rely upon the atgroup of sympatric, relatively closely related tribution of specific morphological characters, for example, tooth dimensions, and jaw primate taxa according to a series of craniorobusticity and shape, to specific, observ- dental variables in order to determine what individual, or combinations of, features are able dietary specializations. The accurate documentation of naturalis- associated with particular dietary prefertic behavior of animals in the wild is a criti- ences. The most useful anatomical comparical prerequisite for determining the func- sons are those between closely related spetional significance of any anatomical cies that exploit either entirely different feature. “Each species of primate has a spe- food sources or the same resources but in cific dietary regime. Each has its own partic- different ways (Fleagle, 1979). Using this ular preferences. These preferences are not approach, the influences of “phylogenetic simply ‘opportunistic’ responses to the food noise” can be separated somewhat from available. Different species feed on different functional adaptation. Platyrrhine primates are particularly things in the same areas” (Hladik and Hladik, 1969, p. 115). In addition, not only well suited for the study of morphological do diets vary according to seasonality of food adaptations to diet because of their preresources, but within classes of foods, that sumptive monophyletic origin, commonality is, fruits, leaves, and animals, variability in of arboreal habitat, morphological variation, food texture (Rosenberger and Kinzey, and variation in food preferences. Although 19761, hardness (Kinzey and Norconk, the feeding behavior of primates has been 1990), and the parts of a particular food re- studied since the 19th century, a recent prosource that are actually consumed (van liferation of field studies now provides conRoosmalen et al., 1988) also contribute to siderable detail for morphological correlates morphological differences among feeding to be better understood for most platyrrhine genera (e.g., Hladik and Hladik, 1969; mechanisms. Features of the cranium, mandible, and Hladik et al., 1971; Izawa, 1975; Klein and teeth, thought to reflect some mechanical or Klein, 1975,1977; Smith, 1977; Fleagle and functional aspect of feeding, are examined Mittermeier, 1980; Mittermeier et al., 1980; for seven genera representing eight species van Roosmalen, 1980; Mittermeier and van of New World monkeys and compared to Roosmalen, 1981; A p e s and Nessimian, their reported naturalistic dietary prefer- 1982; Mittermeier et al., 1983; van Roosences. Each variable considered here has malen, 1980; Terborgh, 1983; van Roosbeen studied, often in isolation, by other malen et al., 1988; Ayres, 1989; Kinzey and workers in order to establish a broader prin- Norconk, 1990; Janson and Boinski, 1992). Using a bivariate approach that focuses ciple relating structure and function, often incorporating a “scaling” perspective that on relative size, or “shape,”the adaptive sigstresses the influence of body size on mor- nificance of individual morphological charphology and adaptation (e.g., Maynard acteristics is interpreted in association with Smith and Savage, 1959; Hylander, 1975a; a relatively detailed documentation of diKay, 1975, 1978; Eaglen, 1984, Bouvier, etary composition. Thus, characters are 1986a,b; Osborn, 1987; Ravosa, 1991). Oth- identified both for species that are someers have focused on a single aspect of feeding what limited in their dietary preferences morphology in two closely related species (e.g., frugivory sensu stricto, seed predation, (e.g., Cole, 1992; Daegling, 1992). The func- folivory) and those that regularly exploit a tional hypotheses generated from these wider variety of available food resources morphological data have been significantly (e.g., omnivory). substantiated by experimentation, collected MATERIALS AND METHODS both on the functional significance of craniLinear measurements of the cranium, omandibular morphology (e.g., Hylander, 1979,1984,1986) and on the forces required mandible, and teeth were taken on 153 dry zyxwvut zyxwv zyxwvutsr zyxwvut zyxwvut zyxwvu DIETARY ADAPTATIOI\IS OF PLATYRRHINES museum specimens from seven genera (eight species) of platyrrhine primates of both sexes: Ateles paniscus (black spider monkey; 4 male, 6 female), Alouatta seniculus (red howler; 12 male, 12 female), Chiropotes satanas (black-bearded saki; 12 male, 12 female), Pithecia pithecia (white-faced saki; 12 male, 11 female), Cebus nigrivittatus (wedge-capped capuchin; 6 male, 6 female), Cebus apella (tufted capuchin; 12 male, 12 female), Saimiri sciureus (squirrel monkey; 12 male, 6 female), and Saguinus midas (red-handed tamarin; 12 male, 5 female). Data from males and females were partitioned when the mean condylobasal length (see below) dimorphism exceeded 5% of the larger sex. The sample was limited to adult specimens that had been collected in the wild. Measurements were taken from the right side of the skull with sliding calipers to 0.001 cm accuracy and reported to the nearest 0.01 cm. The following variables were examined: 1. Condylobasal length-the midline minimum distance from alveolare to a perpendicular tangent to the dorsal margins of both occipital condyleswas measured as an estimate of body size (see below). 2. The length of the incisor row-the linear distance between the lateral margins of the lateral mandibular incisors-was measured to estimate the length of the incisal cutting edge and the wear potential of the mandibular incisor row (Hylander, 1975a). 3. The maximum cross-sectional area of each ipsilateral maxillary and mandibular canine tooth-maximum mesiodistal dimension x maximum buccolingual dimension-was calculated as an estimate of the strength of the tooth. 4. Maximum cross-sectional area of each mandibular premolar and molar (M3 absent in Saguinus m i d a s h t h e mesiodistal diameter between the points of contact with continguous teeth and parallel to the occlusal plane x maximum buccolingual diameter of the crown, normal to the mesiodistal diameter-was calculated and the total area summed as an estimate of masticatory 241 function (Wolpoff, 1971; Kay, 1975, 1978; Pirie, 1978). 5. The lever arms of the masseter and temporalis muscles were measured in order to determine the extent to which masticatory function of a species relies more upon one or the other of these primary jaw elevators. The vertebrate jaw is generally regarded as a Class I11 lever (Davis, 1955; Hylander, 1975b). As such, its fulcrum is presumed to be the temporomandibular joint, with the attachment of the efirortforce (muscles of mastication) situated between the temporomandibular joint and the resistance force (food).The ratio of the lever (or effort) arm to the resistance arm is ordinarily taken as a first-order approximation of mechanical advantage. Because of the close correlation between resistance arm and body size,' and because the resistance arm measurement at any position along the tooth row is independent of the lever arm measurements of either masseter or temporalis, only the lever arm is considered here for comparison of the relative mechanical advantage between muscles in a taxon. a. lever arm of masseter-perpendicular distance from the most caudal extent of the glenoid fossa to a line extending from the midpoint of the attachment site of the superficial masseter muscle along the ventral border of the zygomatic arch to gonion; b. lever arm of temporalis-estimated to be one-half the distance along the Frankfort Horizontal from the most caudal extent of the glenoid fossa to the most rostra1 limit of the temporal fossa on the dorsal aspect of the zygomatic arch (after Demes and Creel, 1988). zy zyxwvu 'Although the data for resistance arm length are not presented here, this variable is highly correlated (r = .99 at prosthion, r = .97 at MI,r = .96 at M,; P < .0001)with condylobasal length. Because the Z-scores (see helow) represent departure from a size prediction based on condylobasal length, the distribution of the mean Z-scores for the lever arms of both muscles are essentially identical to the distribution of mechanical advantage means. zyxwvuts zyxwvu zyxwv F. ANAPOL AND S. LEE 242 6. Mandibular robusticity (depth and breadth) is related to the need to resist compressive, tensile, and shearing forces imposed on the mandible during ingestion and mastication. Mandibular robusticity was evaluated by four measurements: a. Depth of mandibular symphysisinterdentale inferius to gnathion b. Maximum breadth (-thickness) of the mandible a t the symphysis c. Depth of mandible beneath M, d. Maximum breadth of mandible beneath M, 7. The effective height of the mandibular condyle-the perpendicular distance between the highest point on the condyle and the occlusal surface plane of P,-M2 (following Osborn, 1987kwas measured. Among nonprimates, effective condyle height is considerably greater in herbivorous ungulates than in carnivores (Maynard Smith and Savage, 1959). Since specimen body weights were largely unavailable, condylobasal length was the variable chosen to represent body size because it provides a specimen-specific independent variable to be measured directly, thus allowing intragroup ranges to be assessed. This also avoids having to use published mean body weights taken on specimens not associated with the measured sample. Other workers have argued in favor of using some measure of head length for the independent size variable, rather than body mass (e.g., Smith, 1981; Hylander, 1985; Bouvier, 1986a,b; Ravosa, 1990). To justify the choice of condylobasal length as a “surrogate size variable,” mean condylobasal length values (log,) were regressed on the cube root of published body weights’ (log,) of the groups considered here and found to be highly correlated (r = .98, P < .0001; r = .979, P < .0001 when Saguinus midas was excluded from the sample) and close to isometry (least-squares slope of 1.06, 1.09 when Saguinus midas was excluded from the sample; reduced major-axis slope of 1.08,l.ll without Saguinus midas). In order to adjust for size differences among individuals, relative size or “shape” was computed as the residual from isometric scaling or geometric similarity (Falsetti et al., 1993). Using loge-transformed data, an isometric line was forced through the grand means of condylobasal length and the dependent variable using the linear form of Huxley’s (1932) allometric equation Y = bXk: log Y = k log X + log b. To paraphrase Jungers (19881, this approach eliminates most of the variance due simply to body size differences while preserving sizerelated shape information. It should be noted that this is statistically equivalent to Mosimann’s approach to shape variables using logged ratios (Mosimann, 1970; Falsetti et al., 1993). Isometry of masticatory structures is supported, for example, by data on anthropoid muscle weight scaling (Cachel, 19841, anthropoid jaw muscle force by inference (Hylander, 19851, catarrhine incisor scaling (Hylander, 1975a), and anthropoid occlusal area (Kay, 1975,1978). The residuals of individual specimens were standardized by calculating Z-scores with a mean of zero and standard deviation of 1.0. This enables variables to be compared directly regardless of differences in average magnitudes [i.e., whether the deviations are unusually large or small (Smith, 1984; Jungers, 1988)l. Thus, the standardized variables are compared to an a priori size prediction, therefore, largely eliminating the bias present in empirically derived equations (Smith, 1984).A virtually identical distribution was obtained using an alternative methodology in which the Z-scores were calculated from natural log-transformed variables after dividing each raw variable by the condylobasal length. Means and standard deviations were determined for each measured or calculated variable considered in this study and for all Z-scores. Because the Z-scores center every variable relative to the sample mean, a rank order could be generated for each for analysis. While the Z-score cutoff of zero is virtu- zyxwv zyxwvuts - - *Atela paniscus male = 7.86 kg, female 7.69 kg; Alouatta seniculus male 8.53 kg, female = 6.02 kg; Chiwpotes satunas male = 2.98 kg, female = 3.0 kg; Pitheciu pithecia male = 1.87 kg, female = 1.88 kg; &bus nigriuittatus male = 3.5 kg; Cebw upella male = 3.89 kg, female = 3.00 kg; Suirniri sciureus male = 0.74 kg, female = 0.635 kg; Saguinus midas male = 0.492 kg (Fleagle and Mittermeier, 1980). zyxwvuts DIETARY ADAFI’ATIONS OF PLATYRRHINES zyxw zy zyxw 243 TABLE 1 . Estimated relative percantages of fruit mesocarp, seeds, leaves, and fauna consumed by eight species of platyrrhine primates Fruit mesocam Ateles pankcus’ Alouatta seniculus3 Chiropotes satanas‘ Pithecia pithecia5 Cebus nigrivittatus6 Cebus apella7 Saimiri sciureus’ Sapuinus midas’ 84 45 20 47 45 68 77 62 Predated seeds 3 - 75 48 20 7 - 5 Leaves Fauna Other’ - 13 8 - zyxwvu zyxwvu 20 20 18 30 5 5 5 5 5 3 zyxwvutsr ‘“Other” includes relatively minor percentages of fruit, seeds, leaves, insects, buds, twigs, flowers, etc. for which specific figures were not available. Values are based upon van Roosmalen et al. (19881, after adjustment by the following: 2van Roosmalen et al., 1988; van Rwsmalen and Klein, 1989 Kinzey and Norconk, 1990; Strier, 1992. ’Izawa, 1975;Mittermeier and van Rwsmalen, 1981;van Rwsmalen et al., 1988;Neville et al., 1989, after Gaulin and Gaulin, 1982;Ungar, 1990, after Gaulin and Gaulin, 1982, Crockett. 1987, and Crockett and Eisenberg, 1987. 4Boker, 1932; Fooden, 1964; Muckenhirn et al., 1975; Mittermeier and van Roosmalen, 1981; van Roosmalen et al., 1981, 1988; Ayes and Nessimian, 1982; Kinzey and Norcronk, 1990. 5Fooden, 1964; Buchanan et al., 1981;Buchanan et al.,1981, following Hick, 1968;Mittermeier and van Roosmalen, 1981; van Roosmalen et al., 1988; Kinzey and Norconk, 1993. ‘Fooden, 1964; Freese and Openheimer, 1981, after Hladik and Hladik, 1969;Mittermeier and van Roosmalen, 1981;van Roosmalen et al., 1988; Ungar, 1990, after Robinson, 1986 and Robinson and Janson, 1987. ‘Fooden, 1964, Struhsaker and Leland, 1977; Izawa, 1979 Freese and Openheimer, 1981, after Hladik and Hladik, 1969 Mittermeier and van RoosmaIen, 1981;Terborgh, 1983;van Roosmalen et al., 1988;Janson and Boinski, 1992. ‘Fooden, 1964; Izawa, 1975;Baldwin and Baldwin, 1981, aRer Hill, 1960 and Fooden, 1964; Mittermeier and van Roosmalen, 1981. % d e n , 1964; Hershkovitz, 1977, after Crnz Lima, 1945;Mittermeier and van Roosmalen, 1981;v a n b s m a l e n e t al., 1988;Snowdonand Soini, 1989, citing others. ally meaningless in biological terms, the taxa could be analyzed as “relatively larger” vs. “relatively smaller.” Thus, the results are sample specific, whereas the absolute Z-scores (because they are mean centered) would change with the addition or deletion of other taxa. The Z-score rankings were compared to dietary preferences determined from previously documented field studies. The baseline information was that reported by van Roosmalen et al. (1988) for sympatric species observed in the RaleighvallenVoltzberg Reserve in Suriname. Because regional specificity of the museum specimens that were measured could not be controlled while allowing for sufficient sample size, the results from van Roosmalen et al. (1988) were slightly modified as objectively as possible by results published by other authors (see Table 1). Dietary preferences were partitioned into four categories: frugivory, in which the mesocarp of fruit is consumed with the seed either dropped or dispersed endochorically; frugivoryfseed predation, in which the pericarp of fruit is removed and the seed is triturated; frugivoryffolivory, in which leaves (mostly young, flush by preference) are consumed; and omnivory, in which insects or small tetrapods are consumed. The morphological results were compared to estimates of proportions of food types eaten by each species. Pearson’s product-moment correlation coefficients ( r )and the probability ( P ) that r = 0 were also calculated, pairing the mean Z-score for each variable with the estimated arcsin-transformed percentages of fruit mesocarp, seeds, leaves, and animals consumed by each group (Sokal and Rohlf, 1981). These provided an approximation of the relationship between a variable and food type eaten. Computations, statistical analyses, and plots of results were accomplished using SAS (Statistical Analysis System, SAS Institute, Inc., Gary, NC) on a Convex mainframe computer at the University of Wisconsin-Milwaukee. RESULTS Relative percentages of classes of food consumed by the primates considered in this study are presented in Table 1. Values are based on those published in van Roosmalen et al. (1988) and adjusted by results and summaries from other authors. The adjustments did not significantly alter the characterization of any species in terms of its feeding modality. All of these species eat a 244 zyxwvu zyxwv zyxwvut F. ANAPOL AND S. LEE significant proportion of flesh (mesocarp) from available fruit. All but Ateles paniscus supplement their diet with protein, for example, seeds, leaves, and/or small fauna (e.g., insects, birds, small mammals) from at least one other primary food resource. Five of these species (Ateles paniscus, Chiropotes satanas, Pithecia pithecia, Alouatta seniculus, and Saimiri sciureus) regularly consume either fruit flesh almost exclusively or supplemented by only one other major food class. The remaining three species (Cebus nigrivittatus, Cebus apella, and Saguinus midas) are less limited in their food preferences, exploiting more than two food classes in varying proportions. For each measured and calculated variable, means (? standard deviation) of raw values of morphological traits are presented in Table 2. Mean (2standard deviation) Z-scores are shown graphically in Figures 1-7. Considerable sexual dimorphism is present in dental variables of those species for which size, as represented by condylobasal length, merited separate treatment of males and females. Although the larger-bodied males have larger skulls upon which the size variable was measured, they retain teeth that are comparable in size to those of the females (Cochard, 1985). This results in the females having larger Z-scores for all dental variables, except upper and lower canine area. In Alouatta seniculus and Cebus nigriuittatus, the relatively larger canines in the males reduce the Z-score differences between sexes to almost zero. In Saimiri sciureus, and to a lesser extent in Cebus apella, sexual dimorphism in canine area is so pronounced that the males show larger Z-scores than females. With due consideration for (1) the nondietary (e.g., social and defense) functions selecting for larger male body and canine size, and (2) pregnancy and lactation requirements selecting for improved masticatory efficiency in females (Cochard, 19851, we choose to err on the side of conservatism. Therefore, the comparative results for dental characters in sexually dimorphic species are interpreted with regard to the female sample. Correlation coefficients for morphological variables vs. percentages of food classes utilized are referred to when strongly (P < .05) or weakly ( P < .lo) significant. Dental morphology The length of the incisor row (Fig. 1) is relatively longer in Ateles paniscus, Cebus nigrivittatus, Cebus apella, Saimiri sciureus, and Saguinus midas than in Alouatta seniculus, Chiropotes satanas, and P. pithecia. Incisor rowAength (IRL) is strongly correlated with frugivory ( r = .66, P < .03) and faunivory (r = .79, P < .01), and inversely correlated ( r = - .62, P < .04) with folivory. For most groups, upper and lower canine areas (Fig, 2) are closely associated in both the means and standard deviations of their Z-scores. One exception is noted for male Saimiri sciureus, in which the upper canine area is larger than the lower canine area. A lesser disparity is noted for Saguinus midas, in which the upper canine area is slightly less than that of the lower canine. Chiropotes satanas and both species of Cebus have relatively robust canines, while those of Ateles paniscus and Alouatta seniculus are relatively gracile. The canines of P. pithecia and male Saimiri sciureus are intermediate in rank. Upper and lower canine areas are weakly correlated with seed predation ( r = .53, P < .08) and faunivory (upper: r = 3 0 , P < .lo; lower: r = 5 4 , P < .07), while both upper (r = - 5 4 , P < .08) and lower ( r = 5 1 , P < .09) canine areas are inversely correlated with folivory. The total occlusal surface area of the postcanine dentition (Fig. 3) is relatively large in Alouatta seniculus, both species of Cebus, and Saimiri sciureus, while relatively small in Ateles paniscus and Saguinus midas. The pitheciine species are intermediate in rank. This relative distribution of Z-scores is virtually identical for the remaining groups when Saguinus midas is excluded from the data set. When P, and M, areas3 are excluded for all groups, the mean Z-score for Saguinus midas is increased somewhat from -1.40 (k0.52) to -0.75 (20.50) but has negligible effect on the Z-scores for the other groups. In addition to providing longer shearing crests for folivory (Kay, 1975), a greater occlusal area also enables the forces of masti- zyxwvuts zyxwvu zyxwv zy zyxwv 3Total postcanine dentition area is significantly correlated ( r = .79, using raw measurements;r = .60,using Z-scores) with lower canine area (P < .0001). paniscus sciureus sciureus pithecia nigrivittatus nigriuittatus midas seniculw seniculus satanas (F) (M) paniscus sciureus sciureus pithecia nigriuittatus nigriuittatus midas seniculw seniculus (F) satanas (MI (M)(F) (F) (M) (MI(F) (M)(F) (M)(F) (M)(F) zyxwvut zyxwvu zyxwvu zyxwvut zyxwvuts zyxwvutsr zyxwvu 1712 6 1212 6 6 23 24121210 n 1712 6 1212 6 6 2324121210 n lever length Temporalis 116.47 20.63 11.17 16.76 14.09 15.02 16.53 15.73 16.81 13.35 59.95 65.27 68.06 96.82 66.15 89.39 Condylobasal 44.23 73.00 38.45 39.88 74.81 7.58 7.73 8.89 arm (mm) f (mm) f f? 2 f t f ? ? ? C ? ? t c? f t ? _f * * * 0.86 0.94 0.49 0.80 0.94 0.90 1.07 0.85 1.04 1.81 1.17 1.07 2.47 2.50 2.31 3.07 2.67 2.67 3.10 2.07 3.78 6.08 5.53 1.30 TARLE 1712 6 1212 6 6 2324121210 1712 6 1212 6 6 2324121210 n n 2. Grouo Incisor 13.75 13.37 length 12.03 10.57 10.48 11.55 11.37 depth 5.71 22.82 20.97 30.47 26.57 20.65 17.82 16.56 20.73 Symphyseal 6.72 7.84 6.90 8.53 10.10 19.81 11.18 9.35 t t It C t f t t f f f? (mm) rowmeans lr: 2 2 lr: rt f -t ? rt t 2 rt (mm) 0.26 0.44 0.57 0.68 0.57 0.50 0.68 0.78 0.92 0.64 0.50 0.53 01.22 01.48 00.60 00.76 00.39 01.62 00.90 01.31 01.75 01.12 02.59 02.52 1712 6 1212 6 6 2323121210 n 1712 6 1212 6 6 2324121210 n I+ standard Upper 46.84 35.34 34.22 30.34 32.40 areadeviation) 45.23 38.19 30.82 18.51 12.08 6.32 7.58 breadth 10.53 4.28 4.24 9.56 6.70 9.35 7.57 Symphyseal 4.86 8.75 8.00 8.95 8.36* 2 5 ? f? ? t t ? ? t(mm2)canine C f f 2 ? 2 (mm) t5 ? f for 06.86 00.56 03.96 03.64 05.54 03.49 05.11 07.03 08.08 01.73 01.48 10.63 0.60 0.27 0.42 0.98 0.48 0.27 0.30 0.53 0.44 0.49 0.61 1.22 each * * 1712 6 1212 6 6 23 24121210 n 1712 6 1212 6 6 2324121210 n variable Lower depth 32.29 32.00 43.44 28.57 37.98 29.33 areadiscussed 29.01 16.62 10.1145.35 6.57 7.39C 23.57 20.13 14.86 17.91 Corporal 13.88 12.07 16.05 13.98 18.08 6.15 6.82 8.04 at C t t t t f? 2 t(mm2)canine c2 +. t i- f C f f C t 2 2 c (mm)MI in 3.24 4.27 6.16 6.02 5.46 0.75 8.02 3.34 0.94 3.85 2.62 1.58 the 0.79 0.84 0.52 2.40 0.45 0.57 0.81 1.46 1.12 1.42 1.57 1.94 tat 1712 6 1212 6 6 2324121210 n 1712 6 1212 6 6 23 24121210 n breadth 235.52 206.55 area 122.62 112.54 113.59 116.54 Postcanine 21.27 65.67 76.36 39.86 Corporal 34.02k 96.70 4.82 5.75 6.05 2.77 6.42 5.27 7.48 3.03 8.06 7.18f 2.75? 5.76C a t C C f ? ? f f f ? (mm2) f f C t C C c ? t ? (mm) M, 0.68 0.50 0.43 0.20 0.19 0.44 0.43 0.14 0.14 1.00 08.55 22.92 0.41 0.31 05.98 05.94 21.18 11.46 03.16 02.28 03.06 17.22 14.08 12.71 * 1712 6 1212 6 6 2324121210 n 1712 6 1212 6 6 23 24121210 n 246 zyxwvuts zyxwv zyxwvutsrq F. ANAF'OL AND S. LEE zyxwvutsrqponm zyxwvutsrqp zyxwvutsrq zyxwvutsrqponm zyxwvutsr Ateies paniscus Alouatta seniculus F Alouatta seniwlus M Chiropotes satanas Pithecia pithecia Cabus nigrivinatus F Cabus nigrivinatus N Cebus apeiia F Cebus apeiia M Saimiri sciureus F Saimiri sciureus M Saguinus midas 3 -2 0 -1 1 2 3 Z-SCORE (rnean2s.d.) Fig. 1.Mean Z-scores of incisor row length. ( 0 )represents the mean value and the error bars represent one standard deviation above and below the mean. cation on the surface enamel to be more broadly distributed when chewing a wide variety of foods, for example, seeds and the chitinous skeleton of insects. Therefore, the lack of a significant correlation between the area of the postcanine dentition and any single food class, even when P, and M, are eliminated from the calculation of total area, is not surprising. Lever arms of masseter and temporalis muscles (Fig. 4) The difficulty with determining the mandibular attachment (and thus, the lever arm) of the masseter muscle on dry skulls may account for the relatively broad standard deviations of the Z-scores for this variable, by comparison to those of the temporalis muscle. With the exception of male Saimiri sciureus, which has the relatively smallest masseteric lever arm, most mean Z-scores fall within a narrow range (between -1 and 1) and do not markedly partition taxa. By contrast, mean Z-scores of the lever arm of the temporalis muscle are more widely distributed and have considerably smaller standard deviations. These results suggest that the participation of the masseter in chewing is relatively conservative among these species, while the more variable propensity for resisting anteriorly directed forces with the temporalis is more closely linked t o dietary mode. The lever arm length of the masseter is inversely correlated ( r = -.60, P < .05) with faunivory. The lever arm length of the temporalis is strongly correlated ( r = .73, P < .01) with faunivory and inversely ( r = - 5 0 , P < .lo) with folivory. In Ateles paniscus and Alouatta seniculus, and to a lesser extent in Chiropotes satanas and P. pithecia, mean lever arm length of the temporalis is relatively shorter than that of the masseter. In both Cebus species and Saimiri sciureus, the lever arm of the temporalis is relatively longer than that of masseter. In Saguinus midas, the lever arms of both muscles are approximately equal in rank. zyxwv zyxw z DIETARY ADAPTATIONS OF PLATYRRHINES Ateles paniscus 247 zyxwvutsrqp zyxwvutsrqpon zyxwvutsrqp zyxwvutsrqpo Alouafte seniculus F Alouatta seniculus M Chlmpotes salanas Pithecia pithecia ---f &bus nigifvfitafus F &bus nigriviftetus M Cebus apella F &bus apella M Saimiri sciureus F Saimlri sciureus M Saguinus midas -0:. ~~ -3 -2 - zyxwvutsrqpo I I I -1 0 1 7 2 3 Z- SCORE (mean 2 s.d.) Fig. 2. Mean Z-scores of upper (---I and lower (-) canine areas (see Fig. 1 legend). zyxwvuts Mandibular morphology At the mandibular symphysis, overall robusticity (depth and breadth, Fig. 5) is greater in Chiropotes satanas, P. pithecia, Cebus nigrivittatus, and Cebus apella than in the remaining groups. In Saimiri sciureus and Saguinus midas, the corpus is relatively broad for its depth. In Alouatta seniculus, and somewhat less so in Atelespaniscus, the corpus is relatively narrow for its depth. Mandibular depth at the symphysis is strongly correlated ( r = .61, P < .04) with seed predation and inversely ( r = -.63, P < .03) with frugivory. Mandibular breadth a t the symphysis is strongly correlated ( r = .62, P < .04) with seed predation. In the region of M,, mandibular depth and breadth (Fig. 6) are widely disparate in several groups. In Ateles paniscus, Chiropotes satanas, and P. pithecia, the mandibular corpus is markedly deeper than it is broad, with Ateles paniscus having the relatively narrowest corpus of all. The reverse is true for both Cebus species and Saguinus midas, that is, the mandible is considerably broad for its depth. Compared to the female, male Alouatta seniculus has a relatively narrow mandibular corpus for its depth, perhaps an accommodation for a more pronounced acoustic adaptation, that is, to allow sufficient space for the enlarged hyoid bone [the importance of howling to female Alouatta seniculus is thought to be subjugated to that of males (Sekulic, 198211. Mandibular depth at M, is strongly correlated ( r = .71, P < .01) with seed predation and inversely correlated with both frugivory (r = - 5 8 , P < .05) and faunivory (r = -.68, P < .01). Mandibular breadth at M, is weakly correlated with seed predation ( r = 5 0 , P < .lo). The effective height of the mandibular condyle (Fig. 7) over the occlusal plane is considerably greater in Alouatta seniculus than in the other platyrrhine groups considered here. Condylar height is strongly correlated ( r = 34,P < . O l ) with folivory. 248 zyxwvuts F. ANAPOL AND S. LEE Ate/- paniscus zyxwvutsrqpo zyxwvutsrq zyxwvutsrqp Alouatta senicu/us F Aloualta seniw/us M Chiropotes satanas Pithecia pithecia zyxwvutsrqpo zyxwvutsrqpon - Cebus nigfiviltatus F Cebus nigriviiiatus M Cebus apela F ~ e b u sape//a M Saimin' sciureus F Saimiri sciureus M Saguinus midas 1 '---I I -3 -2 -1 0 1 2 3 2-SCORE (rnean&s.d.) Fig. 3. Mean Z-scores of total occlusal area of lower premolars and molars (see Fig. 1legend). zyxwvuts zyxwvutsr Composite Z-score means, calculated as Lucas and Luke, 1984) individual classes of the sum of the Z-score means for all vari- teeth (incisor, canine, premolar, molar) and ables, for each group are arranged in numer- jaw structure often become uniquely elaboical sequence in Table 3. Species having both rated in order to accommodate the exploitathe most varied diets (Cebus spp.) or those tion of one type of food resource over others. In the current study, several sympatric most specialized for the toughest food items (Chiropotes satanas) have the most exagger- genera of platyrrhine primates in the Suriated features, each with a total mean name rainforest, whose naturalistic feeding Z-score >3. They are well separated from behaviors have been relatively well docuthe remaining groups, most of which have mented, are found to exhibit morphological Z-scores <2.5. P. pithecia is the most inter- specializations of the teeth and jaws that mediate form, although showing a negative reflect an adaptative radiation to a wide vatotal. Differences in composite ranking be- riety of available food resources. Although tween males and females of the same species size is not the only determinant of food progenerally are due to differences in their re- cessing, it is relatively easy to measure, can spective Z-scores for the dental variables be manipulated mathematically to reflect shape, and, because it does appear to distin(see above). guish among groups in the sample, provides DISCUSSION some baseline insight into focal areas €or The dentition of primates is generally con- more refined studies of topography. All of the eight species considered herein sidered to be less specialized than that of other mammalian orders. However, due to derive a significant proportion of their calothe physical properties of the foods con- ries from fruit mesocarp. The protein source, sumed (Rosenberger, 1992, after Andrews therefore, appears to be the major determiand Aiello, 1984; Kay and Covert, 1984; and nant of dietary and morphological differ- DIETARY ADAPTATIONS OF PLATYRRHINES Pivlecia pithecia zyxw z 249 zyxwvutsrq zyxwvutsrq zyxwvutsrqp zyxwvutsrqpo _---*--* Cetnis nigMttatus F Cebus nigrivittatus M Cebus apella F &bus apella M I -3 -2 -1 7 7 0 1 .__ z -1 2 3 Z- SCORE (mean? s d . ) Fig. 4. Mean Z-scores of lever arms of masseter (---) and temporalis (-1 (see Fig. 1 legend). ences, with seven species complementing sors indicate the extent to which a form is their diet with at least one other primary frugivorous is well documented (Jolly, 1970; protein resource, for example, seeds, leaves, Hylander, 1975a; Smith, 1981; Cachel, and/or small fauna (e.g., invertebrates, 1983; Eaglen, 1984). Among the platyrrhine species considered birds, small mammals). Thus, four relatively specialized feeding modes are repre- here, relatively wide incisors are found in sented: frugivory (Ateles paniscus), both the dedicated frugivore Ateles paniscus frugivorylseed predation (Chiropotes sata- and in species that consume both fruit mesonas, Pithecia pithecia), frugivorylfolivory carp and significant amounts of animal mat(Alouatta seniculus), and omnivory (Cebus ter (Cebus nigrivittatus, Cebus apella, apella, Cebus nigrivittatus, Saimiri sci- Saimiri sciureus, and Saguinus midas). Relatively narrow, but otherwise specialized, ureus, Saguinus midas). incisors (see below) are found in species in which fruit is supplemented exclusively by Frugivory nonanimal foodstuffs (Alouatta seniculus, Although only slightly smaller than Chiropotes satanas, P . pithecia). The abBrachyteles, Ateles paniscus is much less fo- sence of any single attribute exclusive to livorous (Strier, 1992) and is the most exclu- Ateles paniscus reflects the lack of any spesively frugivorous primate in this sample. cific protein supplementation requiring speIts craniodental morphology emphasizes the cialized preparation by the jaws and teeth. use of a long lower incisor cutting edge for Without closer examination of fine architec“spooning”out chunks of soft mesocarp from tural detail, neither the results presented a wide variety of ripe fruit. That wide inci- here nor gross visual observation permit zyxwvuts 250 zyxwvuts zyxwvu zyxwv zyxwvutsrq F. ANAF'OL AND S. LEE zyxwvutsrqp zyxwvutsrqp zyxwvutsrq zyxwvutsrqpo Ate1e.s paniscus Alouaua seniculus F AlouatEa senlcutus M Chiropotes satanas Pithecie pithecia &bus nigMUatus F Cebus nigMUatus M - -a-- - &bus apela F &bus apella M Saimiti sciureus F Saimiti sciurws M Saguinus mi&s - -3 -2 I I I I -1 0 1 2 zyx 7 3 Z-SCORE (meanksd.) Fig. 5. Mean 2-scores of depth (---) and breadth 1-( legend). large incisor size in the more omnivorous species to be attributed exclusively to either their frugivorous or faunivorous dietary components. By comparison to the other ceboid species represented here, Ateles paniscus possesses a relatively diminutive crushing/grinding masticatory apparatus with which relatively soft foods are processed. The low resistance of ripe mesocarp is reflected by the presence of relatively small canines and cheekteeth and explains why the mandible is also relatively gracile-bone strain recorded directly along the mandibular corpus is correlated to masticatory bite force (Hylander, 1986). In Ateles paniscus, the lever arm of the temporalis is considerably shorter than that of the masseter. This implies increased reliance upon vertically oriented crushing/ grinding forces of mastication per se, and a decreased requirement for resisting anteriorly directed forces ordinarily thought to be of the mandible at the symphysis (see Fig. I associated with faunivory, or at least prehensile use of the jaws for vigorous foraging (see below). That neither jaw robusticity nor postcanine occlusal surface area track the masticatory muscle lever arm ratio in this species reflects the lack of toughness of the foods consumed, that is, eating the soft mesocarp of ripe fruit requires neither strong resistance to anteriorly directed forces nor exceptionally large vertical chewing forces. Frugivory/seed predation The primary food resource of Chiropotes satanas consists of young seeds from unripe fruit that are obtained by removing the tough pericarp with the anterior dentition (van Roosmalen et al., 1988; Kinzey and Norconk, 1990; Kinzey, 1992). The craniodental morphology associated with so-called sclerocarp harvesting (Kinzey, 1992) emphasizes an incisal gouge, large canines, a more equitable balance between temporalis DIETARY ADAPTATIONS OF PLATYRRHINES zyxw z 251 zyxwvutsrqpo zyxwvutsrqpo --- Ateles paniscus Alouatta seniculus F Alouatta seniculus M Chimpotes satanas ~ zyxwvutsrqponmlkjihgfedcbaZYXWVU --c- Cebus nighittatus F Cebus nighittatus M Cebus apella F Cebus apela M Sairnin sciureus F Saimin sciureus M Saguinus midas - -0- -" I zyxwvutsrq -3 -2 -1 0 1 2 3 Z-SCORE (meanr s.d.) Fig. 6. Mean Z-scores of depth 1---) and breadth 1-) and masseter muscle leverage, and a relatively robust mandible to resist the stresses associated with the anterior dentition's habitually being used for opening these kinds of fruits. By contrast to the spatulate incisors of the more dedicated mesocarp feeders, the pitheciine incisors are laterally compressed into a robust procumbent gouge, which is used to liberate the seeds from young unripe tough fruits (Kinzey and Norconk, 1990, after Hershkovitz, 1985). The narrower incisor row effectively concentrates the force imposed upon the cutting edge by the muscles of mastication. The most predominant feature of the dentition of Chiropotes satanas is the exceptionally robust upper and lower canines, also present in both Cebus species studied here. Among large carnivores, the largest canine cross-sectional areas are found in felids and hyaenids, which have more forceful bites (deep killing bites in felids-scavenging in hyaenids) than do canids (shallow bites with of the mandible at MI (see Fig. 1legend). use of molars for crushing bone; van Valkenburgh and Ruff, 1987). For primates harvesting sclerocarp, robust canines provide an advantage for opening exceptionally hard unripe fruits to gain access to seeds (Kinzey and Norconk, 1990). Within the Pitheciini, several features of the jaws and teeth, including canine robusticity, are much less pronounced in P. pithecia than in Chiropotes satanas. Sakis feed upon a wider variety of fruits, and seed predation comprises a smaller percentage of its diet-only -50% of the food resources of P. pithecia, while <86.4% for Chiropotes satanus (van Roosmalen et al., 1988; Kinzey and Norconk, 1990). The resistance of the ectocarp to puncturing in the fruits utilized by Chiropotes satanas (mean 2.77 kg/mm2, maximum 37.80 kg/mm2) average >50% greater than that of the fruits utilized by P. pithecia (mean 1.70 kg/mm2,maximum 5.80 kg/mm2;Kinzey, 1992). How canine size differences between sakis and bearded sakis are possibly influenced by differences in so- 252 zyxwvutsr F. ANAPOL AND S. LEE zyxwvutsrqponm zyxwvutsrqp zyxwvutsrqp zyxwvutsrqpo zyxwvutsrqpo zyxwvuts __c_ Ateles paniscus Aloualta seniculus F Alouatta seniwlus M Chiropotes satanas Pithecia pithecia Cebus nigrivittahrs F Cebus nigriviftatus M Cebus apella F Cebus apella M Saimin' sciureus F Wmin' sciureus M Sagulnus midas - I , -3 -2 0 -1 Z-SCORE (rnean*s.d.) zyxwvutsrqpo 1 7 2 3 Fig. 7. Mean Z-scores of the effective height of the mandibularcondyle (see Fig. 1 legend). cia1 organization remains unclear (Kay et al., 1988). The seeds that are predated by pitheciines are softer than those from the fruits in which the mesocarp is eaten and the seeds either swallowed whole or dropped (Kinzey, 1992). Thus, the crushing/grinding component of trituration can be effected by cheekteeth that are not exceptionally large. Total occlusal surface area is slightly greater in P. pithecia than in Chiropotes satanas. Although both species masticate relatively soft seeds, the larger molar area in P. pithecia may be associated with a greater leaf-eating component (but <lo%) than Chiropotes satanas in its diet (W. Kmzey, personal communication). The size and shape of the mandible is determined by both (1)the texture or hardness of the foods eaten, and (2) where such foods are processed along the tooth row. In the pitheciines, masticatory muscle leverage is somewhat more equitably distributed between the masseter and temporalis than in any other ceboid group, indicating increased use of the anterior dentition for sclerocarp harvesting, without sacrifice of a strong crushinglgrinding capability. In Chiropotes satanas, the moment arm of temporalis is much greater than in the atelines, although both the atelines and the pitheciines have a greater moment arm in masseter than in temporalis. Thus, Chiropotes satanas and, to a lesser extent P. pithecia, are provided with relatively high muscle leverage along the entire length of the mandible. Sclerocarp harvesting is also characterized morphologically by a relatively robust mandibular corpus, as best exemplified here by Chiropotes satanas, and somewhat less so by P. pithecia and both Cebus species, whose diets also include predated seeds. Since the texture of the seeds consumed by pitheciines offers much less resistance than the unripe mesocarp of the fruits in which these seeds are found, their greater mandibular robusticity is more likely due to a fruit-opening rather than chewing function (Kmzey, 1992). When the anterior region of the mandible is loaded, as during incisal gouging of unripe pericarp, bilateral muscle activity imposes both dorsoventral shear and lateral zyxw zy zyxwvutsrqp zyxwvutsr DIETARY ADAPTATIONS OF PLATYRRHINES TABLE 3. For each primate group, the sum of 2-scores (rounded to 0.5) for all variables are arranged by ascension (see Results) 9 (Cebus apella M) 8 Cebus apella (F) 7 6 Chiropotes satanas 5 4 3 2 1 0 -1 Cebus nigrivittatus (F) (Cebus nigriuittatus M) Pithecia pithecia Saimiri sciureus (F) (Saimiri sciureus M) -3 Alouatta seniculus (F) -5 -6 Sanguinus midas lAlouatta seniculus M) -7 -8 -9 mandibular corpus, parasagittal bending during incisal biting is better resisted (Hylander, 19791,thereby decreasing the potential for lost muscle work during biting. Ironically, although the mandibular corpora of the Cebus species included here are relatively thick, they are relatively low in depth. The palm nuts eaten by Cebus apella, however, are much tougher than those eaten by the pitheciines. The broader, shallower corpus may indicate that the seed-opening function is relegated further distally along the tooth row, consequently shifting the emphasis from resistance to dorsoventral bending to resistance to torsion in the postcanine region (Hylander, 1979). Symphyseal robusticity differs markedly between the two pitheciine species. Although the corpus of P. pithecia is relatively robust, the symphysis is intermediately ranked within the sample, well below that of Chiropotes satanas. Because the ectocarp of the fruits utilized by P. pithecia (see above) has a lower resistance to puncturing, the stress on the symphysis during the power stroke of biting (Hylander, 1984) would also be lower. This is also reflected by the presence of relatively smaller canines. A similar requirement for maintaining stiffness in a maximally elongated resistance arm during incisallcanine gouging, however, would serve to maintain a robust corpus in the postcanine region. zyxwvutsr -2 -4 253 Ateles Daniscus zyx transverse bending (“wishboning”) on the symphysis (Hylander, 1984). As the food is Frugivory/folivory transferred distally toward either canine, The primary protein source of Alouatta the stress would be amplified because the balancing side resistance arm would in- seniculus is leaves, preferably young and crease relative to that of the working side, flush. The diet-related morphology of the thus invoking increasingly asymmetrical frugivorelfolivore Alouatta seniculus emapplication of muscle forces. Hylander phasizes the expansion of the postcanine oc(1984) suggests that resistance to both the clusal surface area for chewing tough, fifunction also bending and dorsolateral shear can be bol- brous leafy material-a stered by increasing the depth and thick- assisted by a high effective condyle height ness of the symphysis, observed here in Chi- and greater leverage for the masseter musropotes satanas and both Cebus species. cle than for the temporalis. A relatively reduced incisor row and caSimilar morphological results have been reported previously (Bouvier, 1986b; Daeg- nine area appears to deemphasize use of the anterior dentition concomitant with a correling, 1992). Another consequence of the anterior loca- sponding decrease in parasagittal and tortion of the resistance force is that both bilat- sional bending stresses, as indicated by a eral resistance arms are maximally length- relatively gracile mandible. However, by ened, potentially increasing the vertical contrast t o the spatulate form of the individflexibility of the corpora. By deepening the ual incisors in mesocarp feeders, each inci- 254 zyxwvu zyxwvu F. ANAPOL AND S. LEE sor of the howler monkey tapers mediolaterally toward becoming a point so that force is more highly concentrated on a per tooth basis for biting or pulling off young leaves (Ungar, 1990). Although strongly correlated with shearing, crushing, and grinding features of the molars (Kay and Hylander, 1978), relatively small incisor size may indicate alternative, rather than diminished, requirements for incisal preparation. The narrow incisor rows of sclerocarp-harvesting pitheciines and the folivorous Alouatta seniculus exemplify different solutions by which forces can be concentrated to sustain two widely disparate feeding mechanisms. Among the species in this sample, Alouatta seniculus (and the cebid omnivores, see below) has the largest relative postcanine occlusal surface area. Rosenberger and Strier (1989) reported that Alouattta seniculus has the metrically largest individual molars and largest total postcanine tooth area among representative species of the four extant ateline genera, even larger than that of Brachyteles arachnoides, whose estimated body size [males 9.25-15.0 kg, females 6.912.0 kg, Ford and Davis (1992), citing Ruschi (19641,Aguirre (1971), and Lemos da Sa and Glander (199311 is somewhat greater than that of the red howler. Thus, although folivory is basically correlated to body size among primates (Kay, 1984), despite having a larger body size, Brachyteles does not eat a proportionally greater amount of leaves than Alouatta (Strier, 1992). Both premolar and molar area are known to be correlated to an increased physical resistance of food. In carnivores, broader P3 and P4 occur in extant species that exhibit more bone-crushing feeding behavior than those that eat primarily flesh or flesh and bone (Marean, 1989). Although not directly comparable to the feeding behavior of the primates included here, Marean’s findings do imply a correlation between a premolar dimension and food texture. Large premolar surface area adds to the amount of total grinding surface of the posterior dentition by extending it anteriorly. Molar crown surface area is correlated with bite force (Demes and Creel, 1988) and is a useful measure of masticatory function (Wolpoff, 1971). Thus, greater molar occlusal surface area would be an important safety factor for teeth covered by the relatively thin enamel necessary for the sculpturing of shearing cusps for eating leaves (Kay, 1984) in that the propensity for “wear events”, that is, loss of enamel prisms leading to crack propagation and fracture, would be reduced (Janis and Fortelius, 1988). That both Alouatta seniculus and the omnivorous species (see below) have a relatively large postcanine occlusal surface area reflects the physical similarity between plant fiber and for example, chitinous exoskeletons, both relatively “tough foods (Kay, 1984; Lucas and Luke, 1984). Relatively large molars are generally found in leaf-eating and insect-eating monkeys, and in the grass- and seed-eating Theropithecus (Kay, 1975; Pirie, 1978). The latter eats small food objects, which also entails prolonged chewing but no preparation by the anterior dentition (Jolly, 1970). In contrast to carnivorous mammals, the masseter muscle of herbivores provides the majority of chewing function, thus relegating maintenance of the jaw articulation to the temporalis (Maynard Smith and Savage, 1959). Of the platyrrhines included here, Alouatta seniculus shows (with Ateles paniscus) the highest ratio of masseter to temporalis leverage. Again, this indicates a more pronounced emphasis on producing vertically directed chewing forces, rather than resisting anteriorly directed forces. In contrast to the spider monkey, however, the howler has a more robust mandible, clearly reflecting the disparity in food toughness between relatively soft fruit mesocarp and leaves. Although the lever arm of the temporalis is longer than that of the masseter in cercopithecoid monkeys, the leaf-eating colobines have a larger lever arm in the masseter than do the cercopithecines (Ravosa, 1990). Other features of the masticatory apparatus indicate a preference for masseter muscle use: low coronoid process of temporalis, deep zygomatic arch, expansion of the surface area for attachment of the masseter on the angular (gonial) process (Scapino, 1972), and a low origidinsertion ratio of the masseter (Herring and Herring, 1974). The shape of the ascending ramus of the howler mandible is undoubtedly associated zy zyxwv zyxwvutsr zyxwv zyxwv DIETARY ADAPTATIONS OF PLATYRRHINES 255 zyx zyxwvut with its acoustic adaptation, as reflected by its uniquely cup-like hyoid bone. The effective condyle height, however, was measured above the occlusal surface of the tooth row, while the hyoid is located well below the teeth (Schon, 19711, and is more likely associated with elaborated expansion of the gonial angle than the height of the condyle. Among the primate groups considered here, the effective condyle height clearly distinguishes the most folivorous Alouatta seniculus (Z-score = 1.5-2.0) from the remainder, whose Z-scores fell within a relatively narrow range (= -1.0-0.0). Maynard Smith and Savage (1959) suggest that a high articulation improved the leverage of the masseter and medial pterygoid. However, the height of the condyle over the tooth row may be independent of the mechanical advantage of the masseter (since it does not affect the moment arm) and, therefore, more likely related to bringing the surfaces of the upper and lower tooth rows into occlusion simultaneously, by contrast t o the “scissorslike” occlusion of carnivore jaws (Moss, 1968; Greaves, 1974). Concordant with Moss (1968) and Greaves (19741, the length of the lever arm of masseter in Alouatta seniculus is not substantially larger than in species having a relatively lower condyle height, €or example, Ateles paniscus, Chiropotes satanas, and P. pithecia. In artiodactyl herbivores, increasing the height of the condyle reduces the masticatory pressure exerted by the molars relative to the applied muscular force (DeWolff-Exalto, 1951). Thus, the imposition of lowered masticatory forces over a relatively large molar occlusal area both converge towards a common function of reducing stress on the surface enamel. The implications of this for muscle morphology and recruitment patterns remains unclear. Ironically, the fraction of the combined surface area of the stomach, cecum, and colon, compared to that of the small intestine, places Alouatta seniculus (but not A. palliata) at the center of the range of values for frugivores (Chivers and Hladik, 1984). Thus, the uniqueness of the adaptation to folivory ofAlouatta among the uniformly arboreal New World monkeys suggests that selection initially may, in fact, have been for the acoustic adaptation. Some associated mandibular alterations, including the expanded angular process and low origin/ insertion ratio, may have been preadaptive for leaf-eating, with the remaining cranial and ramal features selected for after the dietary shift to folivory. Omnivory Fauna comprise a large portion of the diet of Cebus nigrivittatus, Cebus apella, Saimiri sciureus, and Saguinus midas. The extent to which omnivory is practiced varies considerably, however, from the more restricted diet of the frugivoreffaunivore Saimiri sciureus to that of Cebus nigriuittatus, which also consumes significant proportions of fruit mesocarp, seeds, and leaves. The craniodental morphology of each of the three omnivorous cebids consists of a constellation of the morphotypic specializations associated with the more limited diets discussed above. All four omnivores have a relatively long lower incisor tooth row, like that of the frugivorous Ateles paniscus. Although this feature, at least in part, reflects the relatively high percentage of soft fruit mesocarp found in their diets, other aspects of the craniodental morphology of these omnivores indicate an adaptation to the resistance of anteriorly directed forces with the implication that other foraging and biting functions also require wide incisors (see below). Both Cebus, along with the seed predator Chiropotes satanas, have the most robust canines of all species presented here, distinguishing them from the other platyrrhine omnivores, Saimiri sciureus and Saguinus midas. However, in contrast to other sympatric species, Cebus (especially Cebus apella) consumes palm nuts with exceptionally hard coats, which are opened with the teeth or by pounding (Struhsaker and Leland, 1977; Izawa, 1979). Saimiri sciureus, for which seed predation is not reported, does not have exceptionally large canines. Upper canine sexual dimorphism (estimated here by comparing the disparity in canine and MI Z-scores between males and females) was greater in Saimiri sciureus than in any other species for which body size merited treating males and females separately. Factors contributing to sexual ca- 256 zyxwvuts zyxwvu F. ANAF'OL AND S. LEE nine-size dimorphism might include differences in male-female feeding andor food procurement (which could not be substantiated for these species), increased levels of within-group breeding competition (Kay et al., 1988), and overall size dimorphism where heritability or phenotypic variability is greater for canines in males than in females (Leutenegger and Cheverud, 1982, 1985). Sexual dimorphism in food procurement or feeding behavior is not known for Saimiri sciureus. Our results can neither substantiate nor disprove the suggestions of Leutenegger and Cheverud. Upper-canine sexual dimorphism was not correlated t o body size-canine size variance dimorphism. The only species in this sample with a greater variance in Z-score for upper canine area was Cebus nigriuittatus, which also had the least sexual dimorphism for this variable. The highest upper-canine dimorphism is found in both the largest (Alouatta seniculus) and smallest (Saimiri sciureus) cebid species in the sample. Concordant with Kay et al. (1988), however, Saimiri sciureus showed greater canine dimorphism than would be expected for competition level 3, with Cebus apella showing much less dimorphism than would be expected for a level-4 group. Small tetrapods and insects provide the greatest diversity in material consistency, much of which is somewhat resistant to trituration, so that the postcanine dentition is relatively large in the cebid omnivores. For Cebus, postcanine use is likely to be associated with the mastication of hard seeds (see below), in contrast to the smaller molars of the pitheciines, which process seeds of much softer consistency (Janson and Boinski, 1992; Kinzey, 1992). Cebus apella also has exceptionally thick molar enamel, by comparison to other species reported by Kay (1981). Other (molar) features of Cebus species (C. capucinus) suggest adaptation to a highly plastic, but nonfolivorous diet (Rosenberger and Kinzey, 1976). The lever arm of the temporalis is greater than that of the masseter in the three cebid omnivores, thus separating them from the remainder of the sample. The relatively larger lever arm of the cebids' temporalis, affected by their relatively high coronoid process, not only increases its mechanical advantage for raising the mandible but, by directing its line of action more anteriorly also permits posterior inclination of the muscle without sacrifice of mechanical advantage (De Mar and Barghusen, 1973; Bramble, 1978). Furthermore, primates that emphasize incisal preparation of food have a relatively high anterior temporalisl masseter muscle weight index, as reported for adult Saimiri sciureus and Cacajao rubicundus (Cachel, 1979). Thus, resistance to large anteriorly-directed forces is maximized by increasing both the lever arm and the effort force of the temporalis. In carnivores (sensu stricto),the temporalis typically obtains a greater mechanical advantage for resisting the anteriorly directed forces of struggling prey, while the masseter assists by preventing dislocation of the temporomandibular joint (Maynard Smith and Savage, 1959). Although the small fauna [mostly invertebrates, some small vertebrates, including some mammals s 1 kg (Robinson, 198611 eaten by these cebids hardly requires the highly specialized prey-capture prehensility found in the feeding apparatus of large cats hunting ungulates, the analogous distribution of leverage may nonetheless be explicable in terms of their foraging techniques. The largest disparity between masseter and temporalis in lever arm length is found in Cebus. The foraging behavior of Cebus apella is relatively destructive and entails pulling with the teeth and hands to break open dead branches while hunting for hidden prey in tough substrates (Terborgh, 1983; Janson, 1985; Janson and Boinski, 1992). Terborgh (1983) noted that the magnitude of the destructive behavior decreases with size from Cebus apella, through C. albifrons, to Saimiri, which has a relatively smaller lever arm length in temporalis than Cebus. Cebus nigriuittatus is only slightly smaller in body size than Cebus apella and probably uses its jaws in a similarly vigorous manner. The disparity in lever arm length is markedly less in Saimiri sciureus than in Cebus. Its presence in the squirrel monkey may be attributable to their habits of plucking fruit zyxwvu zyxwvutsr zyxw zyxw DIETARY ADAPTATIONS OF PLATYRRHINES by the mouth, in contrast to the manual plucking by Cebus, and eviscerating larger (>2 cm) caterpillars (and perhaps other species as well) by pulling their head and viscera out with their mouths while holding the prey in the hand (Janson and Boinski, 1992, citing Boinski and Fragszy, 1989). Of further interest is the sexual dimorphism in lever arm ratios present in Saimiri sciureus: In males, the lever arm of masseter is relatively shorter, while the lever arm of temporalis is relatively longer than in females. This provides males with a larger gape and is probably linked to their having relatively larger canines than females. The large gape may merely be a mechanical requirement for canine tip clearance during mastication or a further enhancement of their display behavior during intermale competition. Unlike either Saimiri sciureus or Saguinus midas, both Cebus species have relatively robust mandibles, reflecting their propensity for seed predation. This is slightly more exaggerated in Cebus apella, despite having a smaller percentage of predated seeds in their diet. The difference, however, likely results from the unique dependence of Cebus apella on habitual exploitation of palm nuts, which are highly resistant to opening as well as to chewing. Fully ripe palm nuts are not eaten by other sympatric primates (Izawa, 1979). Cebus apella has a more robust symphysis and corpus, and eats harder foods than either C. capucinus (Daegling, 1992) o r C. albifi-ons (Cole, 1992). Saguinus midas presents a paradoxical case in that, despite a diet that includes not only fmit and insects but some seed predation as well, the incisor tooth row is the only feature showing a positive Z-score-in all other variables, Saguinus midas ranked relatively low or intermediate. Because the size and toughness of foods chosen by tamarins is limited by incisal capacity and gape, little adaptive pressure exists for exaggeration of any of the other morphological features that characterize dietary specializations of the larger species. A similar principle may dictate the extent to which body size determines a species’ ability to adapt locomotorwise t o a two- or three-dimensional environment. As Jenkins (1974) points out, 257 the arboreallterrestrial dichotomy may be artificial to the small tree shrew because the relatively cluttered forest floor presents the same impediments to locomotory behavior as is encountered in the trees. By analogy, for a tamarin, which is relatively small by comparison to the size of the foods exploited-because incisal biting reduces every food item to a manageable size, alteration in the size of specific craniodental components may be subject to little selective pressure. CONCLUSIONS (1)Frugivory, as represented by Ateles paniscus (>80% fruit mesocarp eaten), is associated with a long incisor tooth row as its predominant morphological adaptation. The remaining craniodental variables are either relatively small or of average size in this species; no variable is relatively large in the frugivorous Ateles paniscus exclusively. (2) Species that supplement their diet with a single nonanimal protein resource display diagnostic features that reflect the class of food exploited, such as seeds or leaves: (a) Frugivorylseed predation, as represented by Chiropotes satanas (and somewhat less so by P. pithecia), is best characterized by exceptionally robust canines and mandibles. The division of labor between the primary jaw elevators, masseter, and temporalis, is relatively balanced, with the lever arm of masseter only slightly greater than that of its synergist. (b) Frugivorylfolivory, as represented by the howler monkey Alouatta seniculus, is best characterized by an exceptionally high mandibular condyle, similar to that found in nonprimate herbivores, and a relatively large poscanine dentition. (3) Omnivory, as represented here by Cebus apella, C. nigrivattatus, and Saimiri sciureus, is best characterized by the presence of a long incisor tooth row, a large postcranial dentition, and better muscle leverage in temporalis than masseter. The Cebus species also have relatively robust canines and mandibles, reflecting that a substantial proportion of their calories is obtained from pre- zyxwvut 258 zyxwvu zyxwvut zyxwvutsr zyxw F. ANAPOL AND S. LEE dated seeds, a dietary Source not exploited gracile-jawed saimiri sciureus. by the (4) Diminutive such as midas, emphasize incisal biting of a variety of food resources (e.g., fruit, seeds, fauna). The necessity to reduce all foods to an ingestibly manageable may relax sesize in lection pressure for iodental features other than incisor row length. ACKNOWLEDGMENTS We would like to express our appreciation to paula jenkins of the British M~~~~~ of History (London) and Dr' Bruce Patterson of the Field Museum of Natural History (Chicago) for access to the Primate collections; to Drs. Gene Albrecht, Herbert Barghusen, Walter Greaves, William J ~ warren ~ K ~ ~ K~~~~ ~~ strier, ~ ~ Christopher Wood, and three reviewers for helpful discussions and advice; and to Craig Engleman, Bob Read, and Frank Stetzer for critical technical assistance. This work was funded by a grant from The University of Liverpool Research Development Fund RDF 560 to F. Anapol. Bouvier M (1986b)Biomechanical scaling of mandibular dimensions in New World monkeys. Int. J . Primatol. 7:551-567. Bramble DM (1978) Origin of the mammalian feeding complex: Models and mechanisms. Paleobiology 4.m1-301. Buchanan DB, Mittermeier RA, and van Roosmalen MGM (1981) The saki monkeys, genus Pithecia. 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