AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 88~499-514(1992) Dietary and Dental Adaptations in the Pitheciinae WARREN G . KINZEY Department of Anthropology, City College, and the Graduate Center, City University of New York, New York,New York 10031-9198 KEY WORDS Dental morphology, Feeding adaptations, Callicebus, Aotus, Pithecia, Chiropotes, Cacajao ABSTRACT Since Mivart (1865), Cacajao, Chiropotes, and Pithecia have been grouped into a single taxon, which he called the subfamily Pitheciinae but which I, following Rosenberger (this issue), refer to as the living members of the tribe Pitheciini. While few today doubt the association of these three living genera, not all would place them together with Aotus and Callicebus in the subfamily Pitheciinae. This is an attempt to sort out the behavioral and morphological features of feeding and dental morphology in these taxa. Extant members of the tribe Pitheciini are adapted for sclerocarpic foraging, morphological evidence for which is found in the fossils of Soriacebus and Cebupithecia. Sclerocarpic foraging in living pitheciins is a two-stage process of seed predation involving 1)specialized features of the anterior dentition that allow removal of a hard pericarp that protects a seed or seeds, followed by 2) mastication by the posterior dentition having low cusp relief to triturate nutritious seeds of a relatively soft and uniformly pliable consistency. The dentitions of fossil pitheciins, Soriacebus and Cebupithecia, demonstrate that the hypertrophy of lower incisors plus the robustness and flaring of the canine precede development of low cusp relief on molars and premolars in the evolution of morphological features associated with sclerocarpic foraging. Features of sclerocarpic foraging are found less uniformly in the other two pitheciines, Callicebus and Aotus. o 1992 Wiley-Liss, Inc. Living primates in the subfamily Pitheciinae (Rosenberger 1981, 1992; Rosenberger et al., 1990) include the traditional pitheciins, Pithecia, Chiropotes, and Cacajao in the tribe Pitheciini, together with Callicebus and Aotus. All these monkeys are primarily frugivorous-as are most neotropica1 primates-and there is now considerable evidence that the former three are seed predators, frequently on unripe fruit with relatively hard pericarps (Ayes, 1986,1989; van Roosmalen et al., 1988; Kinzey and Norconk, 1990,1992); the latter two genera consume very few seeds. The purpose of this study is to bring together dietary and dental evidence on all five genera to determine the degree to which they share derived features related to feeding and foraging. A stimulus for this analysis came from research of Rosenberger, who suggested that 0 1992 WILEY-LISS, INC among the extant platyrrhines Cacajao, Chiropotes, Pithecia, Callicebus, and Aotus form a monophyletic group (Rosenberger, 1981,1988).Virtually all taxonomists, from early to recent times, have recognized the monophyly of of the first three of these: the sakis and uakaries. Older classifications, however, generally did not recognize any special relationship between the sakiuakaries on the one hand and Callicebus andlor Aotus on the other. Based primarily on characteristics of the dentition, Rosenberger (1979) first suggested that all five genera share a suite of derived features. Subsequently, Robinson et al. (1987) grouped these five genera in their review of social adaptations. Received July 11,1990; accepted December 10,1991, 500 W.G. KINZEY According to Robinson et al. (19871, the five genera share both morphological and behavioral features. For example, they have a narrow range of body weights from about 1 to 4 kg and very little sexual dimorphism in body size, and (with the exception of Cacajao and Chiropotes) they live in small groups. Groups of both Chiropotes (van Roosmalen et al., 1988; Norconk and Kinzey, unpublished data) and Cacajao (Ayres, 19891,however, frequently subdivide into smaller foraging groups. If there are dental features uniting these primates, then the features should reflect similarities in feeding adaptations. This assumes that a relationship exists between dental morphology and foraging behavior-a relationship that is consistent with evolutionary theory. This paper demonstrates similarities and differences in feeding and foraging behavior, relates these behavioral features to features of dental morphology, determines which features are symplesiomorphic (primitive) and which are synapomorphic (shared, derived), and suggests a unified hypothesis of consistent morphology, phylogeny, and behavior. The traditional tripartite subdivision of primate feeding categories into fruit, leaves, and animal prey (see, e.g., Kay, 1973, 1984) disregards meaningful categories such as “exudativory”and “omnivory”as well as critical distinctions within these categories, a point also made by Rosenberger (1992).This definitional problem is most apparent within the category “frugivory,”wherein important adaptive distinctions must be made between at least two different kinds of fruit eaten by nonhuman primates: those whose seeds are dispersed by the primate without predation of seeds and those whose seeds arepredated by the primate. The contrast is especially useful from the plant’s point of view, since the primary evolutionary consideration of a plant is dispersal of its seed. The contrast is also useful from the animal’s point of view, since major biomechanical factors involved in ingesting and masticating (see Kinzey and Norconk, 1992, for definition of terms) divide along similar lines. Plant seeds must be dispersed by some method, and at least three-fourths of primary rain forest fruit are dispersed by animals (van Roosmalen, 1985). The contrast between seed dispersal and seed predation hinges on who eats the fruit; thus the distinction here is only made with respect to the nonhuman primate. Dispersed fruit When a primate disperses seeds it digests the pericarp,’ usually the mesocarp, and/or the aril. The fruit may be dehiscent, especially if the aril is the part consumed. Dispersed fruits are soft when ripe and generally are ripe when eaten. Incisor preparation during ingestion accounts for relatively broad incisors in some frugivores (Hylander, 1975). The seed is protected from predation by its own hardness (mechanical resistance to crushing) and/or by chemically resistant testa. Mesocarp commonly has low levels of available protein, which therefore must be obtained from nonfruit resources, usually animal or leaf protein. This category includes zoochorous fruit types 1-4 of van Roosmalen (1985). Usually, the seed passes through the digestive tract (endozoochory) protected by its adherent testa, or it may be spit out (Corlett and Lucas, 1990) or dropped without passing through the digestive tract (synzoochory).Primates, such as Ateles, together with birds, are the major dispersers of seeds of this type of fruit in the neotropics. In the Old World tropics, seed dispersion may differ; in Borneo, Leighton (1992) found that primates, bats, and birds tended to disperse seeds of different fruit species. Predated fruit Seeds of fruit in this category are protected by mechanical and/or chemical means. Fruit may be hard or soft, depending on whether the protection is mechanical or ’The pericarp, drived from the wall of the ovary, is the wall of a fruit that surrounds a seed or seeds. It is subdivided into a n outer exocarp (e.g., the “skin” of a peach or apple); a middle mesocarp, usually the fleshy part of a fruit; and an inner endocarp. The endocarp is the hard covering that protects the seed offruits such as Licania (Chrysobalanaceaeb An aril is another type of seed covering. It is the fleshy derivative of the stalk of the ovule, usually bright-colored, most often found in dehiscent fruit, to attract a seed disperser with a nutritious reward for dispersing the seed. An example is mace (red when ripe) that covers a nutmeg seed. The innermost seed covering (i.e., the seed coat) is the testa, derived from the integument of the ovule itself. The testa usually protects a seed from digestive enzymes when it is swallowed whole by a bird or mammal. In the case of Brazil nuts (Bertholletia ercelsal, the testa is the hard woody covering of each individual nut. 501 PITHECIINE FEEDING ADAPTATIONS Aotus Callicebus Pithecia I Chiropotes Cacajao Tribe Pitheciini Atelinae Tribe Aotini Subfamily Pitheciinae Fig. 1, Interrelationships of the Pitheciinae. (Adapted from Rosenberger, 1988,with permission of the editors.) chemical, and may become harder or softer with ripening, depending on whether chemical protection decreases or increases with maturation. In all cases the seed, with its high level of fat andlor protein, is the nutritionally desirable item for the primate. When a primate digests a seed, it usually obtains higher quality protein than it would if it digested only the mesocarp, so seed predators generally consume relatively few insects or young leaves as obligate sources of protein. When protected mechanically the outer covering (pericarp, usually the endocarp, andlor sometimes the seed coat) is hard and the animal must utilize some specialized means of opening the fruit, usually large canine teeth. If the fruit is protected chemically, the animal must have some means of detoxifying toxic secondary compounds. All three pitheciin primate genera (the saki-uakaris) are predispersal seed predators (Janzen, 1971) and sclerocarpic harvesters (Kinzey and Norconk, 1990) and eat fruit predominantly from this category. These fruits (type 5 of van Roosmalen, 1985) are normally dispersed by rodents after the fruit falls to the ground. Whether sakiuakaris are generally capable of detoxifying secondary compounds is yet to be determined, although there is some evidence that Pithecia can tolerate moderate levels of condensed tannins (Kinzey and Norconk, 1992). SHARED DERIVED DENTAL FEATURES IN THE PlTHECllNAE Figure 1 shows the taxonomic relationships proposed by Rosenberger, and Table 1 lists shared (presumably derived) dental features a t each node. There are features shared only by Cacajao and Chiropotes; another set of features is shared among the Pitheciini (Cacajao, Chzropotes, and Pithecia);and a third, smaller set is shared by all five taxa. These features are found both in the anterior dentition (canine and incisors) and in the molars. A more extensive list of shared dental traits in the three living Pitheciini, together with convergent conditions 502 W.G. KINZEY TABLE 1. Shared derived dental characters’ I. Chiropotes-Cacajao 1. 12 reduced compared with I’ 2. C1 greatly enlarged, especially in female 3. P4 molariform (“subrectangular” as opposed to “suboval”) 4. Reduced lingual cingulum on upper molars 5. Protoconulid present (thus increasing the crushinglgrinding area with the hypocone) 11. Pitheciini (Chiropotes, Cacajao, Pithecia) = “pitheciins” or saki-uakaries 1. Proclivious upper and lower incisors 2. Styliform and high 11-2 crowns 3. 11.2 lingual heels absent 4. Splayed, enormous upper and lower C 5. C1 lingual crest sharp 6. Female Pz massive and projecting 7. P3-4 hypoconids large 8. P4 strongly molarized 9. Molar enamel surface crenulate 10. Stong preprotocristid 11. Postprotocristid 12. Ectoflexid reduced 13. Trigonid elevation = that of talonid 14. Robust jaws 111. Pitheciinae (Chiropotes, Cacajao, Pithecia, Callicebus, Aotus) = “pitheciines” 1. 11-2 height increased (and cingulum lost), and relatively large roots 2. Lingual tubercle on I’ (not Aotus) 3. Enlarged lingual cingulum on C’ (not Aotus) 4. Large hypocone (possibly symplesiomorphic) 5. P4 strongly molarized (not fossil Cebupithecia) 6. Distal fovea on M1-2 (not Aotus) ‘Kinzey (1973), Rosenberger (1979), Ford (1986), Kay (1990). in other taxa, may be found in Kay (1990). If shared derived dental features represent adaptive features in feeding, then there should be a link between dental characters and diet. Within the Pitheciinae, Chiropotes and Cacajao are the two largest genera (Ford and Davis, 1992) and share a number of derived features in both the anterior and the posterior dentition (Table 1).In the anterior dentition the upper lateral incisor is reduced, probably in relation to occlusion with the very narrow lower incisors. They clearly demonstrate the most exaggerated “pitheciin” characteristics, which are further described below. Of the three groups of taxa listed in Table 1, the members of the Pitheciini share the largest number of derived features, including unique cranial (Rosenberger, 1979) and postcranial (both forelimb and hind limb) (Ford, 1986) characters and immunological (Cronin and Sarich, 1975; Baba et al., 1979) and cortical (Falk, 1980) features. The close relationship of these three genera has been recognized since Mivart first grouped them together in the Subfamily Pitheciinae in 1865. Their monophyly has been recognized by most, if not all, who have subsequently studied Neotropical primates (e.g., Hill, 1960; Hershkovitz, 1977; Ford, 1986; Kay, 1990; Rosenberger, 1992). Derived features in the anterior dentition of the Pitheciini include characters of both incisor and canine (Table 1).The lower incisors are extremely styliform (see Fig. 21, and both upper and lower incisors are inclined anteriorly from root to tip of crown, forming an efficient nipping or cropping device. In the pitheciins, the most remarkable shared dental feature is the enormous, laterally splayed canine. The canines are of greater height and caliber than is expected relative to body size and relative to the length of the postcanine dentition (Orlosky, 1973; Rosenberger, 1979; Anapol and Lee, 1990). In Chiropotes, the virtual lack of sexual dimorphism in dental morphology (Swindler, 1976; Hershkovitz, 1985) suggests that the robust canine is related to feeding and not to social behaviors. Canine enlargement is related to use in breaking open hard fruit. The canine teeth, unlike those of other ceboids, are buccolingually tapered (Hershkovitz, 19851, which produces a wedge-like morphology with well-developed cutting edges on mesial and distal surfaces of both uppers and lowers. The combination of these features results in the canine being functionally separated from the incisors in two ways. First, in both jaws, a diastema isolates the canine from the lateral incisor. Second, the orientation of the canine cutting edges differs from that of all other ceboids in that they have rotated medially, being positioned outside the contour of the dental arcade. This frees the canines from interference with the incisors when used for puncturing large food items and facilitates puncturing a hard object with considerable force. Derived features in the posterior dentition of the Pitheciini include characters of both premolars and molars (Table 1).The Pt (last premolar) is enlarged and molariform, and both Pi and P$ frequently have crenulated occlusal surfaces. The low occlusal relief and the presence of crenulations on all three up- PITHECIINE FEEDING ADAPTATIONS 503 Fig. 2. Anterior dentition of the five Pitheciinae, with Ateles for comparison. a: Cacajao rnelunocephulus, USNM 256217. b: Chiropotes satanus chiropotes, USNM 338964. c: Pithecia pithecia, USNM 339658. d Callicebus torquatus lugens, USNM 406416. e: Aotus grisimembra, USNM 396796. f: Ateles belzebuth hybridus, USNM 443388. per and lower molars are hallmarks of the pitheciins. Some have suggested that the specialized molar morphology (in Caccijao [Ayres, 19891 and Chiropotes [van Roosmalen et al., 19881) is related to chewing hard food items. Rosenberger and Kinzey (19761, however, suggested that by analogy with phylostomid bats the low occlusal relief is related to chewing relatively soft dietary items. Recent field evidence of feeding in both Chiropotes satanas (Kinzey and Norconk, 1990) and Pithecia pithecia (Kmzey et al., 1990; Kinzey and Norconk, 1992) suggests that, after opening fruit with hard husks by using robust canines, pitheciins are, in fact, masticating relatively soft, pliable seeds. Probably a combination of a seed's consistency and its hardness provides the most important selective pressure for molar morphology. Most seeds masticated by Pithecia and Chiropotes have an even, smooth, pliable consistency. Once the pericarp, together with a hard endocarp (if such is present), is removed with the anterior dentition, the material presented to the mo- lars has a smooth, even texture. The molar and premolar crenulations that accompany reduced cusp relief in pitheciins probably serve to facilitate secondary breakdown of seed particles during grinding (Phase I and 11-type chewing movements) (Lucas and Luke, 19841, so grinding, rather than crushing per se, may be the major function of the low relief of pitheciin molars. Crenulations also may aid in containing deformation of seeds that are hard and resilient as opposed to hard and brittle. Recent studies of enamel microwear (Kay, 1987; Runestad and Teaford, 1990), enamel thickness (Maas, 1986; Dumont, 19901, and enamel microstructure (Maas, 1986, 1988) shed some light on pitheciin dental function but also seem to cloud the issue (temporarily, one hopes). Kay (1987; corroborated by Runestad and Teaford, 1990) noted that Chiropotes had relatively more pits (and fewer scratches) on wear facet 9 of M, (a crushing facet) than did Ateles. He suggested that toughness or hardness of ingested food is correlated with the Chiropotes 504 W.G. KTmZEY wear pattern, reflecting mastication of hard-shelled fruit rather than mature (soft) fleshy fruit. It is known that “hard-object feeders” are characterized by high proportions of pits (Teaford, 1985, 1988; Teaford and Walker, 1984), but the answer is not that simple. Pits and striations may represent opposite ends of a continuum, characterized by varying degrees of compression and shear during occlusion (Gordon, 1982). Since maximum intercuspation is probably reached relatively early during mastication of soft foods (Hiiemae, 1976,1978;Hylander et al. 1987; Thexton et al. 19801,Ateles may be using primarily puncture-crushing mastication (during which teeth fail to approach intercuspal range [Hiiemae and Kay 19731) to reduce soft fruit and may consequently produce few pits and large numbers of scratches from shearing. Chiropotes, on the other hand, masticates seeds thoroughly before swallowing, irrespective of their hardness, resulting in large numbers of pits. It is not altogether clear that the pitlscratch distinction between Chiropotes and Ateles is simply the consequence of the former eating hard items and the latter eating soft ones. The nature of the masticatory process must be considered. It is significant in this regard that, in museum collections, Ateles molars tend to be much more heavily worn into the dentin than are Chiropotes molars (personal observation). The low occlusal relief of the latter probably resists wear (Rosenberger and Kinzey, 1976), especially from objects such as seeds (whether hard or soft) that are not brittle, rigid, stiff, fibrous, inelastic, or unyielding. In fact, the seeds that Chiropotes and Pithecia chew have a lower resistance to crushing than do seeds that are swallowed by Ateles (Table 2). Seeds masticated by Pithecia and Chiropotes do not therefore fit neatly into one of the three food categories suggested by Lucas and Luke (1984). They may be soft or hard, but they are not brittle. Maas (1988) demonstrated that forces greater than 10 kg are generally necessary to produce pits, and Kinzey and Norconk (1990) provided data to show that maximum crushing resistance of seeds masticated by Chiropotes satanas was 22 kg, which correlates with the presence of pits. On this basis, one would expect large pits on the molars of TABLE 2. Crushing resistance (in kg) of whole seeds of species of fruit swallowed b y Ateles paniscus a n d masticated b y Chiropotes satanas and b y Pithecia pithecia Number of species of fruit N Range (kg) Average (mean f s.e.) Chiropotes’ Pithecia2 Ateles’ 19 17 13 86 0.2-22.3 7.2 f 0.66 165 0.5-37.0 10.8 k 0.74 65 1.4-148.2 17.1 jI 2.64 ‘Kinzey and Norconk (1990). ‘Kinzey and Norconk (1992). Pithecia pithecia as well, since maximum crushing resistance of seeds masticated by Pithecia was 37 kg (Table 2). Preliminary studies indicate that Chiropotes exhibits strong enamel prism decussation-another feature possibly indicative of “hard” object feeding. The enamel of two Chiropotes upper molars (Maas, 1986; Kinzey, unpublished data), however, is thin, less thick than that of Alouatta and no thicker than that of Ateles. Also, Maas (1986) found that enamel decussation in platyrrhines is independent of enamel thickness. Thick enamel in Cebus (Kay, 1981; Maas, 1986; Dumont, 1990) is probably related to the requirement of molars to masticate hard brittle objects (Kinzey, 1974),such as the chitin of insects: Enamel is thick because abrasion is severe. Those pitheciin molars that have been examined thus far, on the other hand, show thin enamel but strong horizontal decussation: resistance to crack propagation rather than resistance to abrasion. This follows from the suggestion of Maas (1988) that characteristics of microwear are not simply a matter of force and may reflect a variety of factors, including force vectors and enamel microstructure. Further study is needed to sort out the interrelationship of these factors in pitheciines. A third set of shared dental characters (Table 1)is found in the subfamily Pitheciinae: the three genera discussed above plus Callicebus and Aotus. Some dental characters are shared only by the first four genera. Other characters, including three derived postcranial traits (Ford, 1986), Calticebus alone shares with the pitheciins. In the posterior dentition, large hypocones are found in molars of all five genera; PITHECIINE FEEDING ADAPTATIONS however, this may be a symplesiomorphic character for the Ceboidea. Most of the premolar and molar features that Callicebus shares with the Pitheciini are not found in Aotus (Table 1);posterior dental synapomorphies are clearly most pronounced in the Pitheciini. A more significant adaptive link among the five pitheciine genera is seen in features of the anterior dentition (see Fig. 2). Increased height of incisors and the development of mesiolingual cusps on upper central incisors (except in Aotus), together with enlarged roots, suggest important use of the incisors during feeding. Callicebus (torquatus) frequently use their incisors to scrape the mesocarp from palm fruit such as Jessenza bataua (personal observation). The incisors of Aotus wear heavily and flat from marked utilization (Kinzey, 1974). In the pitheciins, the incisors have become even more specialized by narrowing and forming a gouge. While the case for shared derived dental features is much stronger for the pitheciins, a number of shared morphological features in the Pitheciinae do indicate a n adaptive affinity. It is significant that the more developed shared features in the Pitheciinae are found in the anterior dentition: it is the anterior dentition that is expected to evolve sclerocarpic foraging features first (see under “Evolutionary Relationships” below). These similarities may, of course, be the result of convergence or shared phylogeny. 505 TABLE 3. Puncture resistance (in kg/mm2) of fruit species eaten by Chiropotes satanas, Pithecia pithecia, and Ateles paniscus Number of species of fruit N Range (kg/mm2) Average (kg/mm2) Chiropotes’ Pithecia2 Ateles’ 34 17 26 231 0.03-37.8 2.77 198 0.01-6.8 1.70 132 0.03-1.4 0.58 ‘Kinzey and Norconk (1990). ‘Kinzey and Norconk (1992). only in undisturbed upland (nonflooded) forest; Cacajao is only found in flooded forest (both igapo and uurzea) (Ayres, 1989) but may move into terra firme forest during the dry season (Barnett and da Cunha, 1991). Chiropotes only very rarely comes to the ground. Pithecia is the most adaptable of the three pitheciins; is found in both flooded and nonflooded forest, both disturbed and undisturbed habitats; and is sympatric with both Chiropotes and Cacajao. There is no single feature of the habitat shared by all genera. All five genera of Pitheciinae are known to feed primarily on fruit, from roughtly 5580%in Callicebus and Aotus to 90%or more in Pithecia, Chiropotes, and Cacajao (see Table 4). No primate is 100%frugivorous; fruit, by itself, does not generally provide adequate lipid and protein. Figure 3 illustrates the relative proportions of fruit, leaves, and insects in the diets of extant primates. The pitheciines as a group, and especially the pitheciins, are among the most frugivorous FEEDING AND FORAGING IN New World primates and tend toward foliTHE PlTHECllNAE vory more than toward insectivory. Insects are a consistently small and insigFor the most part, pitheciines tend to have nificant portion of the diet in pitheciines, distinct habitat preferences (Robinson et al., 1987). Although Aotus is versatile, occupy- with two exceptions. Aotus supplement their ing all strata of the forest canopy, it is the frugivorous diet with a significant percentonly nocturnal anthropoid (Wright, 1989). age of insects, and this is probably related to Callicebus torquatus is found only in vegeta- increased insect availability in the nocturtion on white sand soils (Kinzey and Gentry, nal niche. Callicebus torquatus has a signif1979), although the other species of titi mon- icant percentage of insects in its diet, replackey are more versatile. C. brunneus and C . ing sclerophyllic leaves in large part. This is cupreus’ have been observed primarily at related to its living on nutrient-poor soils, lower levels in the canopy (Kinzey, 1981). which promote a high level of toxic comWith few exceptions, Chiropotes is found pounds in leaves (Kinzey and Gentry, 1979). Wright reported that Callicebus brunneus spent 15%of “feeding” time foraging for insects, but “due to low capture efficiency, in‘Terminology for species of Cullicebus follows Hershkovitz (1990). sects are not a significant portion of their 506 W.G. KINZEY TABLE 4. Annual percentages of items in the diets of pitheciine primates’ Suecies Pithecia albicans Pithecia hirsute Seeds2 39 38 Other fruit 30 55 Leaves -Flowers Pithecia hirsuta Pithecia pithecia 18 53 33 60 16 0 Pithecia pithecia Pithecia pithecia 17 61 62 X Pithecia pithecia (dry season) (rainy season) Chiropotes albinasus Insects X X References Johns, 19863 Soini, 19864 (1-14) (25-68) (38-88) 0 3 30 4 28 (3-51) 14 7 (1-13) 2 (0-15) 0 1 (1-6) Happel, 19825 Mittermeier and van Roosmalen, 19816 Oliveira et al., 19857 Kinzey and Norconk, 1992’ Setz, 19879 ? ? 36 55 77 32 54 X 19 0 3 11 0 3 X Ayres, 19891° 11 3 X X Ayres, 198111 van Roosmalen et al., 1 0 Kinzey and Norconk, 6 5 Ayres, 198614 (12-82) Chiropotes satanas Chiropotes satanas 63 66 9 30 <5 Chiropotes satanas 91 6 1 Cacajao calms 67 18 Aotus nigriceps (20-97) X X 198812 199013 X 75 5 X (0-94) 15-20 Wright, 1985, 198915 33 2 11 15 Wright, 198516 Wright, 1985, 198917 Kinzey and Becker, (60-100) Aotus azarae Callicebus brunneus X X 16 40 54 28 Callicebus personatus ? 81 18 1 0 Callicebus torquatus 37 30 13 X 14 (22-64) 19A3” Kinzey, 197719 ’Seasonal (monthly) ranges of percentages are given in parentheses when known. Totals do not always add to loo%, since other dietary items, e.g., bark, are excluded. A “X” indicates that the food item was reported being eaten, but rarely, and a percentage was not given. ‘Includes fruit (e.g., whole fruit) from which seeds were known to be predated. ”Based on 54 feeding observations collected over a total of 72 hr, at Lake Tefe, Brazil. ‘Based on a full year of data collected in the Pacaya-Samiria Reserve, Peru. 5Percentages of “bouts” (=“an individual chewingor ingesting a given food”), not percentages of timespent feeding on a given food; data collected during a brief dry season, 12 km north of Puerto Bermudez (Pasco), Peru. ‘Pithecia was only rarely observed, and sample sizes are “quite small.” Data collected a t Raleighvallen-Voltzberg Reserve, Suriname. 7Based on 29 feeding observations during 45 days in January and August on the left bank of the Rio Negro, 30 km west of Manaus, Brazil. ‘Based on 86 days of observations over 16 months in a 3 ha forest fragment in eastern Venezuela. Percentages are based on 10,119feeding minutes. ’Based on 133 hr in July (dry season) and 135 hr in March (rainy season) in a 9.1 h a forest fragment, 85 km north of Manaus, Brazil. Percentage of feeding bouts given for total fruit consumption, which was not subdivided into seeds and nonseeds. “Based on 128 feeding observations over 17 months on Rio Aripuans (MT), Brazil. “Based on 189 feeding records collected on 48 occasions over 3 months (September, January, April), 23 km north of Manaus, Brazil. ”Based on 217 feeding observations over 2.5 years at Raleighvallen-Voltzberg Reserve, Suriname. I3Based on 2,141 feeding minutes observed over 6 months at Raleighvallen-Voltzberg Reserve, Suriname. I4Based on 2,345 feeding records observed over 20 months a t Lake Teid, Brazil. ”Based on observations over 15 months in tropical moist forest a t Cocha Cashu, Peru. [Previously referred to a s Aotus triuirgatus Hershkovitz, 1983).] ‘6Based on 430 hr of observations over 4 months in dry, subtropical forest in the chaco, Paraguay. [Previously referred to as Aotus triuirgatus (Hershkovitz, 1983).] I7Based on 4 full days of sampledmonth for 11months in tropical moist forest a t Cocha Cashu, Peru. [Previously referred to as Callicebus rnoloch (Hershkovitz, 1990).] The only seeds eaten and chewed were those of Brosirnurn alicastrurn (ranked sixth in feeding minutes). Percent insects is based on time spent “foraging,”and “due to low captureefficiency,insects arenot a significant portion of their diet during most of the year” (Wright, 1985:68); “Only 13%[of feces samples] were found to contain insect parts” (Wright, 1985:69). “Based on 2 months of observations during the dry season in tropical Atlantic coastal forest in Espirito Santo, Brazil. ”Based on data collected during 3 months in tropical moist forest, Mishana, Peru. diet during most of the year” (Wright, 1985:68), and “only 13%[of scat samples] were found to contain insect parts” (Wright, 1985:69).Evidence for insect feeding was recently reviewed for Pithecia (Heymann and Bartecki, 1990) and for Chiropotes (Frazao, 1991). The most frequent supplement to the pitheciine frugivorous diet is leaves andor flow- ers (including nectar). Leaves are a major supplement in Aotus, Callicebus personatus, and C. brunneus. All three have molars with well-developed shearing crests (Kinzey, 1978, personal observation). During the dry season, when fruit was scarce, C. brunneus increased its consumption of leaves, especially new growth of liana leaves and bamboo shoots, to 64% of feeding time (Wright, Leaves Insects Leaves Kay, 1984 Fruit Fig. 3. Comparison of diets of the Pitheciinae with those of other primates, showing relative proportions of fruit, leaves, and insects in the diet. Triangle at the right after Kay (1984). Aotus Callicebus Pithecia Chiropotes Cacajao Pitheciinae Fruit Insects A =apes C = cercopithecines L = lorises M = malagasyprimates 0 = colobines @= platyrrhines SYMBOLS COMPARISON OF DIETS OF THE PlTHECllNAE WITH THOSE OF OTHER PRIMATES W.G. KINZEY 508 TABLE 5. Seed predation as a percent o f feeding time (range o f monthly averages) Species Percent seed predation Cacajao caluus Chiropotes satanas 20-97 63-91 Chiropotes albinasus Pithecia pithecia 12-82 17-88 Pithecia hirsuta Callicebus torauatus Callicebus brunneus Aotus azarae 18-68 37 Rare' Rare' References Ayres, 1986 Ayres, 1981; van Roosmalen et al., 1988; Kinzey and Norconk, 1990 Ayres, 1989 Mittermeier and van Roosmalen, 1981; Oliveira et al., 1985; Kinzey and Norconk, 1992 Happel, 1982; Soini, 1986 Kinzev. 1977 WrigGt; 1985 Wright, 1985 'Seeds of Bronsimum alicastrum (Morsceae) only. 1985).Pithecia and Chiropotes both supplement their frugivorous diet with leaves, although C. albinasus may be an exception.p . pithecia, in eastern Venezuela, fed on leaves every month of the year, and leaves were a small but consistent portion of the diet virtually every day (Norconk and Kinzey, 1990; Kinzey and Norconk, 1992). Leaves appeared to be a minor portion of the diet of Cacajao caluus, but stomach contents of two animals captured in December at Lake Teiu contained -60% leaf material (Ayres, 1989). Although none of the pitheciins have anatomical specializations of the gut associated with folivory (Ayres, Chivers, and Johns, in Johns, 1986),Milton (1984) determined that Pithecia monachus had an unusually long food passage rate, which may facilitate the digestion of leafy material. Pithecia appears to be the most folivorous of the pitheciins and also has the least reduction in molar occlusal relief. The most significant dietary item consumed by all the pitheciins is seeds (Table 5). In times of resource stress Pithecia, Chiropotes, and Cacajao all increase consumption of seeds in their diets. Cacajao does so except during a brief interval when virtually all fruit is absent from the trees. At this time, Cacajao descended to the ground to obtain seeds of seedlings, which they dug out of the ground and ate (Ayres, 1990). In the varzea, terrestrial frugivorous competitors are absent. Monkeys that are spending such high percentages of their feeding time on fruit must be gaining something from the fruit that other frugivores are not. That something is seeds, which are particularly high in protein andor lipid. Cacajao (Ayres, 1986), Chiropotes (Kinzey and Norconk, 19901, and Pithecia (Kinzey and Norconk, 1992) all use their canine teeth for opening hard, tough fruit to obtain seeds. Whole fruit, with a diameter of at least 5 cm, can be held by Chiropotes between upper and lower canines on one side of the mouth and sufficient pressure applied until the fruit is broken open. Fruit with puncture resistance up to 38 kg/ mm2 (Kinzey and Norconk, 1990) has been opened by Chiropotes satanas in this manner. Measurements of resistance to puncturing are available for fruit consumed by Chiropotes and Pithecia (Table 3). Fruit eaten by both Chiropotes satanas and Pithecia pithecia were considerably harder on average than the hardest fruit eaten by spider monkeys, which were sympatric with Chiropotes. Quantitative field data are not available for Cacajao, but Ayres (1986) reported that C. caluus opened the hardest shells of immature fruit to obtain seeds, and the most preferred seeds eaten were from fruit with hard husks. At the onset of a long-term study of C. melanocephalus, Barnett and da Cunha (1991) reported that golden-backed uacaris were seen feeding predominantly on fruit with hard husks. The ability of pitheciins to open the hard pericarp of fruit to obtain nutritious seeds is a critical function (Rosenberger and Kinzey, 1976) of the anterior dentition of these animals. High puncture resistance of the pericarp appears to be negatively correlated with high crushing resistance of seeds among fruit eaten by Pithecia and Chiropotes (compare Tables 2 and 3 ) .The average resistance of seeds crushed by Pithecia was 10.8 PITHECIINE FEEDING ADAPTATIONS * kg 0.8, and the average for Chiropotes was only 7.2 & 0.7 kg (see Table 2). Thus, compared with Chiropotes, Pithecia eats fruit whose pericarp has lower resistance t o puncturing (hence the less robust canine) and whose seeds have higher resistance t o crushing. Pithecia molars should show features more highly correlated with crushing (vis-a-vis grinding) compared with Chiropotes. Among species of fruit whose seeds were masticated by Pithecia and Chiropotes, the maximum crushing resistance of whole seeds was 37 kg. They are much softer, for example, than seeds swallowed by Ateles (Table 21, which have a maximum crushing resistance of 148 kg. As a point of reference, the maximum occlusal force generated in humans between molars in white U.S. males was 91 kg and that in male Eskimos was 158 kg (Bourne, 1982). There is evidence that both Pithecia and Chiropotes prefer soft over hard seeds. An important fruit resource of both saki monkeys includes the seeds of Chrysophyllum lucentifolium (Sapotaceae). Pithecia often come to the ground to obtain these fruit. The average crushing resistance of Chrysophyll u m seeds from fruit picked from the tree and dropped by Pithecia was 30 kg, whereas the average resistance of seeds obtained from fruit on the ground was 10 kg. Preferred seeds of this species apparently become softer after remaining on the ground for a period of time. Chiropotes, which rarely come to the ground, drop Chrysophyllum fruit, sometimes after they have removed and eaten most of the seeds. The average crushing resistance of seeds remaining in such fruit fragments was 2 kg; the average of seeds in fruit which had been bitten into, but from which no seeds had been removed, was 23 kg (unpublished data). Although comparable data are not available for Cacajao, Ayres (1986) points out that in C. c. caluus terrestrial foraging for seeds during times of fruit scarcity is a striking aspect of its ecology. It is also possible that seeds obtained from fruit on the ground pose a lower risk of toxicity than those obtained from fruit in the tree. Seeds from Chrysophyllum and Capparis fruit picked up from the ground by Pithecia have virtually no condensed tannins (Kinzey and Norconk, 1992), 509 but comparable data are not yet available from fruit in the tree. Plants frequently protect seeds with secondary toxic compounds as well as hard seed coats. Whether any of the pitheciine primates is capable of detoxifying such toxins is not yet known. However, Pithecia masticated seeds of Licania that contained as much as 9.9% condensed tannins (Kinzey and Norconk, 1992). Although it appears that seed predation in this group of monkeys is the result of specialization to obtain seeds that are protected by hard seed coats, especially at early stages of fruit development, detoxification of secondary compounds may also be a significant factor in obtaining nutrients from seeds. If seed predation is a major evolutionary adaptation of the Pitheciini, then to what extent do Callicebus and Aotus share this tendency? They have not traditionally been regarded as seed predators. Furthermore, the field data imply that seed predation is rare, although not in Callicebus torquatus (Table 5). Even though seed predation is rare in Callicebus brunneus and Aotus, the particular time when they do consume seeds of fruit such as Brosimum is significant. Brosimum alicastrum is a large emergent, which produces large quantitites of very nutritious drupes (single seeds within a relatively hard covering formed by the inner part of the mesocarp) over a short period of time. When fruit is fully ripe in such a tree, the tree’s canopy may be filled simultaneously with at least six primate species and at least 20 avian species feeding together on the abundant resource (P.C. Wright, personal communication). However, Callicebus behave differently, virtually never feeding in a tree in which other primates are feeding. Titi monkeys, living in small family groups, find adequate food in large emergent trees, such as Brosimum, even when fruit is just beginning to ripen (Wright, 1985bwhen only small numbers of drupes are present and these are mostly unripe and generally harder in consistency than ripe fruit. A similar situation was seen when C. brunneus fed in a large fig tree with a 35 m-wide canopy (Fig. 4).These data lead to the suggestion that the pitheciin specializa- 510 W.G. KINZEY 5 4 2 I Phenology 1 July 7 14 21 28 I 7 August Fig. 4. Feeding time (midday) of Callicebus brunneus in a fig tree (Ficus erythrosticta) during JulyAugust, 1981, as a function of fruit availability. (Phenology, shaded area: 5 = maximum fruit available; 0 = no fruit available). Cocha Cashu, Peru. (Courtesy of P.C. Wright.) tion of eating hard-husked fruit began in a such as palm fruit, from which they obtain species living in small groups, as selection relatively hard mesocarp (in the case of favored the ability to obtain harder, less ripe Scheelea) or the nut (in the case of Astrofruit (as does Callicebus brunneus) without caryurn) (Terborgh, 1983; see also Janson competition from sympatric frugivores. This and Boinski (1992). Cebus, as an adaptation adaptation has been elaborated in Pithecia to eating hard, brittle objects, have develand to a greater degree in Chiropotes and oped thick enamel on their molars; pitheciines, as far as we know, have thin enamel Cacajao . In summary, dietary differences between on their molars and are crushing occasionmost of the Pitheciinae (especially the pith- ally hard but always more elastic, nonbrittle eciins) and other platyrrhines appear to be food items. In this sense, seed-bearing fruit related primarily to the high proportion of eaten by pitheciin primates during times of seeds in their diets. Of the potential primate fruit scarcity (and unavailable to other pricompetitors for seeds, only Cebus occasion- mates lacking the anterior dental specialally incorporate seed eating (in contrast to izations) may be considered a “keystone reseed dispersal) into their diet. The signifi- source” (Terborgh, 1986). Avian seed cant difference for C. apella, a hard-object predators (e.g., macaws, parrots) may reprefeeder (Kinzey, 1974), is that they either use sent a more important class of seed competimanual skills to open hard husks (Peres, tors for pitheciins than other primates. We 1991) or use their thick enameled molars for have referred to this adaptation as sclerocrushing hard, inelastic, or brittle items carpic foraging (Kinzey and Norconk, 1990), PlTHECIINE FEEDING ADAPTATIONS which enables pitheciin primates to obtain otherwise inaccessible nutritious (and frequently soft) seeds by breaking through the hard pericarp. EVOLUTIONARY RELATIONSHIPS The fossil record suggests a separation between the Homunculini (Aotus, Callicebus, * T r e m a c e b ~ s , Homunculus, ~ *Xenothrix) and Pitheciini (Pithecia, Chiropotes, Cuca. * J ~ O , Cebupithecia, "Soriacebus), since a t least Friasian (middle Miocene) times, about 15 million years ago (mya) (MacFadden, 1990; Rosenberger, 1992). Evidence for their being distinct at the taxonomic level of the tribe includes behavioral [nocturnality (Aotus),tail twining (Callicebus),especially high incidence of seed predation (Chiropotes, Cacajao)]and morphological (large orbits (Aotus), small canines (Callicebus), compressed lower incisors (Pithecia, Chiropotes, Cucajao)] specializations of each group. Other evidence, presented here, suggests a possible association among these taxa in both behavioral and morphological features of diet and dentition. (See Kay, 1990, for an alternative view.) If the development of sclerocarpic foraging in the Pitheciini began by the Friasian, probably as a specialization for small groups to feed on early-ripening, hard fruit with nutritious seeds, we should see some morphological evidence for this in the fossil record. Neither Soriacebus nor Cebupithecia demonstrate the exaggerated low relief of molars found in extant pitheciins. On the other hand, Soriacebus [Pinturas Formation, Santacruzian age, 18-15 mya (MacFadden, 1990); two species (Fleagle, 199011 shares with the living Pitheciini lower incisors that are procumbent and compressed mesiodistally, with large incisor roots, and robust lower canine; however, C1 is not separated from I,, nor is it laterally flared. Cebupithecia, even more than Soriacebus, exhibits pitheciin incisor procumbency and canine eversion and robustness. Thus both fossils exhibit pitheciin features in the anterior dentition. Both Soriacebus (Fleagle, 1987; Kay, 1990) and Cebupithecia (Hershkovitz, 1970) 'Fossrl taxa are identified by an asterrsk. 511 have been regarded as nonpitheciines, largely on the basis of their lacking pitheciin molar characteristics. On the contrary, this is what one would expect if sclerocarpic foraging was evolving among early pitheciins. Sclerocarpic foraging in living pitheciins is a two-stage process of seed predation involving, first, removal of hard pericarp, followed by mastication of the seed. Thus the requisite anterior dental morphology for opening tough husks would logically have developed first, and only subsequently, after sclerocarpic foraging had become firmly established, would molar specializations, adapted for improved processing of seeds, have developed. Setoguchi et al. (1988) also recognized the distinction between anterior and posterior dentitions of Cebupithecia and suggested that the molars were representative of omnivory. Thus hypertrophy of the anterior dentition is the key to unraveling the origin of sclerocarpic foraging in the pitheciins. Hypertrophy of lower incisors is the one synapomorphic character of all living and fossil Pitheciinae; however, Tremacebus lower incisors are unknown, and broken Homunculus incisors must be assumed to have been heightened. Therefore, until better fossil evidence of the anterior dentition of the Homunculini is known, it seems best to limit the discussion of the evolution of sclerocarpic foraging to the Pitheciini. In its least developed form (e.g., Callicebus), the increased height of lower incisors provides a slightly more efficient means to obtain fruit. In its most developed form (Chiropotes and Cacajao), together with the hypertrophied canine, it is a highly specialized mechanism for opening tough pericarps. The scenario reflected in the fossil record suggests that the initial adaptation included development of incisor height and lateral compression together with canine robustness (Soriucebus).This would have allowed increased advantage in opening small, hard fruits. Second, the canine enlarged and developed flare, increasing the advantage of opening larger fruit (Cebupithecia). A decrease in occlusal morphology of the molars produced the fullblown adaptation. Thus Cebupithecia demonstrates the development of sclerocarpic foraging capability in the anterior dentition of pitheciins of the Colombian W.G. KINZEY 512 La Venta fauna by Friasian times; Soriacebus, from the earlier Argentine Pinturas Formation, is more problematic, as was pointed out by Kay (1990) and Fleagle (1990), having developed sclerocarpic features only in the incisors. However, whether Soriacebus is a pitheciin or not, it has the expected anterior dental features of a n incipient sclerocarpic forager. If it is not a pitheciin, it has developed incipient sclerocarpic foraging characteristics through convergence. This is not a perfect scenario; the least specialized living pitheciin, Pithecia, retains low molar relief but has less well-developed canines (see Fig. 2). I t may be that Pithecia has become adapted secondarily for a more varied diet and depends less on robust canines for opening tough husks than do Cacajao and Chiropotes. The progressive sharing of derived characters from Callicebus to Pithecia to Chiropotes and Cacajao represents a morphocline of increasingly specialized features for fruit husking and seed predation-sclerocarpic foraging or harvesting in the living Pitheciinae. Relative to dietary and dental adaptations, phylogenetic relationships among these taxa will be clarified by additional study of microscopic features of the enamel, by more detailed examination of their ability to detoxify secondary compounds in seeds, and by additional paleontological and behavioral field work. ACKNOWLEDGMENTS I thank Elena Cunningham, Paul Gerber, Scott A. Mori, A.L. Rosenberger, and Karen Strier for critical comments on earlier drafts of the manuscript; Patricia Wright for providing Figure 4; and Ian Carmichael for sectioning teeth for microscopic examination of enamel. I a m grateful to Dr. Richard W. Thorington, Jr., for permission to examine and photograph specimens in the U.S. National Museum. 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NOTE ADDED IN PROOF A new genus of pitheciin primate, roughly contemporaneous with Cebupithecia, was recently described by Meldrum and Kay a t the 61.4 annual meeting of the American Association of Physical Anthropologists [Am. J. Phys. Anthropol. Suppl. f4:121 (199211. With its “procumbent styliform incisors” it further strengthens the suggestion that specialization of the anterior dentition preceded reduction of molar occlusal relief in the evolution of sclerocarpic foraging.