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Dietary and dental adaptations in the Pitheciinae.

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Dietary and Dental Adaptations in the Pitheciinae
Department of Anthropology, City College, and the Graduate Center, City
University of New York, New York,New York 10031-9198
Dental morphology, Feeding adaptations, Callicebus, Aotus, Pithecia, Chiropotes, Cacajao
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
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,
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.
Tribe Pitheciini
Tribe Aotini
Subfamily Pitheciinae
Fig. 1, Interrelationships of the Pitheciinae. (Adapted from Rosenberger, 1988,with permission of the
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).
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
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
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-
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
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
of fruit
Range (kg)
(mean f s.e.)
7.2 f 0.66
10.8 k 0.74
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;
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
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.
TABLE 3. Puncture resistance (in kg/mm2) of fruit
species eaten by Chiropotes satanas, Pithecia pithecia,
and Ateles paniscus
Number of
species of fruit
Range (kg/mm2)
‘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
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
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
sects are not a significant portion of their
TABLE 4. Annual percentages of items in the diets of pitheciine primates’
Pithecia albicans
Pithecia hirsute
Leaves -Flowers
Pithecia hirsuta
Pithecia pithecia
Pithecia pithecia
Pithecia pithecia
Pithecia pithecia
(dry season)
(rainy season)
Chiropotes albinasus
Johns, 19863
Soini, 19864
Happel, 19825
Mittermeier and
van Roosmalen, 19816
Oliveira et al., 19857
Kinzey and Norconk,
Setz, 19879
Ayres, 19891°
Ayres, 198111
van Roosmalen et al.,
Kinzey and Norconk,
Ayres, 198614
Chiropotes satanas
Chiropotes satanas
Chiropotes satanas
Cacajao calms
Aotus nigriceps
Wright, 1985, 198915
Wright, 198516
Wright, 1985, 198917
Kinzey and Becker,
Aotus azarae
Callicebus brunneus
Callicebus personatus
Callicebus torquatus
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
’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,
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,
Kay, 1984
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).
A =apes
C = cercopithecines
L = lorises
M = malagasyprimates
0 = colobines
@= platyrrhines
TABLE 5. Seed predation as a percent o f feeding time (range o f monthly averages)
Percent seed
Cacajao caluus
Chiropotes satanas
Chiropotes albinasus
Pithecia pithecia
Pithecia hirsuta
Callicebus torauatus
Callicebus brunneus
Aotus azarae
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
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),
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-
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),
which enables pitheciin primates to obtain
otherwise inaccessible nutritious (and frequently soft) seeds by breaking through the
hard pericarp.
The fossil record suggests a separation between the Homunculini (Aotus, Callicebus,
* T r e m a c e b ~ s , Homunculus,
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
Both Soriacebus (Fleagle, 1987; Kay,
1990) and Cebupithecia (Hershkovitz, 1970)
'Fossrl taxa are identified by an asterrsk.
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
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
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.
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. Collection of unpublished
data reported here was supported by NSF
grants BNS 87-19800 and 90-20614.
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A new genus of pitheciin primate, roughly
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the 61.4 annual meeting of the American
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dietary, dental, pitheciin, adaptation
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