(Pitheciidae)
Class: Mammalia
Order: Primates
Family: Pitheciidae
Thumbnail description
Diverse family of small- to medium-sized monkeys with long, thickly haired tails (except Cacajao) and long, coarse or dense hair (except Chiropotes), which range in color from white, buffy, yellow, and orange to brown, black, gray, and agouti
Size
Length: 9.1–21.7 in (232–550 mm); weight: 1.5–7.6 lb (700–3,450 g)
Number of genera, species
4 genera; 28 species
Habitat
Highland and lowland rainforest, tropical dry forest, liana forest, savanna forest, mountain savanna forest, secondary forest, igapó, várzea, swamp, gallery forest, and disturbed habitat
Conservation status
Critically Endangered: 2 species; Endangered: 1 species; Vulnerable: 9 species; Data Deficient: 2 species
Distribution
Found in South America in the Amazon and Orinoco basins, Atlantic coastal forest of Brazil, parana forests of Bolivia and Paraguay
Evolution and systematics
The platyrrhine family Pitheciidae includes four genera in two subfamilies. The subfamily Pitheciinae includes sakis (Pithecia, 5 species, 5 subspecies), bearded sakis (Chiropotes, 2 species, 3 subspecies), and uakaris (Cacajao, 2 species, 5 subspecies). The subfamily Callicebinae includes only titi monkeys (Callicebus, 19 species, 5 subspecies). The genus Pithecia is further subdivided into two groups: the Pithecia pithecia group containing two subspecies of Pithecia pithecia, and the P. monachus group (P. monachus, 2 subspecies; P. irrorata, 2 subspecies; P. albicans, and P. aequatorialis). Callicebus is also further subdivided. Prior to Hershkovitz's revision of the genus in 1990, only three species were recognized. Taxonomies published in 2000 and 2001 modify his revision, listing 19 species in four species groups: the Callicebus modestus group (1 species), the C. donacophilus group (4 species), the C. moloch group (12 species), and the C. torquatus group (2 species, 5 subspecies). Callicebus taxonomy is in a state of flux.
The saki-uakari group has long been considered a distinctive adaptive radiation and titi monkeys have usually been considered a sister group to it based on both morphological and genetic evidence. Previous classifications have also considered night monkeys (genus Aotus) a sister group to the pitheciins, but as of 2001, this genus has been place in its own monogeneric family.
Several fossil primates from early Miocene localities in Argentina (Soriacebus, Proteropithecia, Homunculus, Carlocebus), Middle Miocene localities in Colombia (Cebupithecia, Nuciruptor), and Quarternary localities in the Caribbean (Xenothrix, Antillothrix, Paralouatta) have been aligned with both the Pitheciinae and the Callicebinae. Earlier forms are more primitive and not readily aligned with any extant taxa, but it is possible to identify lineages leading to extant pitheciins in later forms.
Physical characteristics
Pitheciids are small- to medium-sized monkeys. Callicebus is the smallest, followed by Pithecia, Chiropotes, and Cacajao. Both Chiropotes and Cacajao are sexually dimorphic in size, with males 20–23% larger than females. Sexual dichromatism is uncommon, but is found in Pithecia pithecia and P. aequatorialis.
It is most pronounced in Pithecia pithecia: males are solid black with a white face and black nose, while females are blackish-agouti with white stripes from under each eye to the corners of the mouth.
Other pitheciids range in color from dark agouti with paler hands and feet and sex-specific patterns of facial hair (Pithecia species), black with light to dark brown back and shoulders (Chiropotes satanas), silky black with a white nose (C. albinasus), reddish orange to orange, or white (Cacajao calvus), or black with a reddish brown to orange back, belly, and thighs (Cacajao melanocephalus). Callicebus is a very diverse genus in terms of coloration. The pelage ranges from black hands (Callicebus personatus), or black all over with yellow hands (Callicebus torquatus), while other species vary from agouti to roufous to grayish with various facial markings.
The four genera are quite distinct in appearance. Pithecia and Cacajao have long, coarse, fluffy hair, Callicebus has long, dense, fluffy hair, while Chiropotes is distinctive in having short body hair. Pithecia and Chiropotes have long, bushy, nonprehensile tails, Callicebus has a long, thickly haired tail, and Cacajao is unique in having a short, bushy haired tail that measures only one-third the length of its body. Distinctive beards, bulbous temporal swellings, and distinctive pink scrotums in males and pink vaginal lips in females characterize bearded sakis (Chiropotes). The bald uakari (Cacajao calvus) is unique in having a bright red, naked face and a bald head
The major defining feature of pitheciids is a shared dental complex. Enormous laterally splayed canines that are functionally separated from the incisors by a diastema are used to open fruits protected by hard, thick husks. The incisors are inclined anteriorly for cropping fruit, and the lower ones are styliform. The molars have low occlusal relief and crenulations. Pitheciids have been characterized as "sclerocarpic foragers" because of their specialization for exploiting heavily protected fruit, such as species of the Brazil nut family (Lecythidaceae).
Distribution
All four pitheciid genera are only found in South America. Callicebus has the largest distribution, inhabiting tropical forests in the Amazon and Orinoco basins (C. moloch and C. torquatus groups), the Atlantic coastal forest in Brazil (C. personatus), and the parana forests of Bolivia and Paraguay (C. donacophilus). The two Pithecia species groups are separated by the Amazon River, with the Pithecia pithecia group found in the Guiana Shield north of the Amazon River and east of the Rios Negro and Orinoco, and the P. monachus group found south of the Amazon and west to the Andean foothills. Chiropotes is found north of the Amazon in the Guiana Shield and between Rios Xingu and Garupi south of Amazon (C. satanas), while C. albinasus is found south of the Amazon in Brazil west of the Rio Xingu. The two species are not sympatric. The genus Cacajao is restricted to western Amazon flooded forests, with Cacajao calvus inhabiting inundated forests south of the Amazon on whitewater rivers (várzea) in Brazil and Peru, while C. melanocephalus is only found in inundated forests on black-water rivers (igapó) north of the Amazon in Brazil and Venezuela.
Habitat
All pitheciid species are predominately or exclusively arboreal, but habitat use by the four genera is variable. Both Pithecia and Callicebus are found in a wide variety of habitats. Pithecia species are found in highland and lowland forests, tropical dry forest, igapó, high várzea, secondary forests, disturbed habitats, liana forest, savanna forest, and mountain savanna forests. Callicebus species are found in inundated forests, swamps, and river and lake edges (C. moloch), open canopy in mixed, gallery, evergreen, and tall forests near streams (C. torquatus), and secondary but not primary forest with low canopy, thickets, and vine tangles in the Atlantic Coastal rainforest (C. personatus).
Both Chiropotes and Cacajao are found in fewer habitat types. Chiropotes species are restricted to terra firme, high rainforest, high mountain savanna forest, savanna forest, and high moist forest. They have not been observed in lowland, disturbed, secondary, flooded, or gallery forests. Cacajao species are found almost exclusively in igapó and várzea, but have been observed to seasonally migrate to terra firme forest.
Behavior
Pitheciid social organization is quite variable. Callicebus is unique among pitheciids in exhibiting a pair-bonded, monogamous social structure, living in groups of 2–6 individuals (adult couple and offspring). Pithecia species live in small multimale/multifemale groups. Chiropotes lives in multimale/multifemale groups of 10–30 individuals with a roughly equal sex ratio, while Cacajao lives in large multimale/multifemale groups of up to 100 individuals.
Grooming behavior is important in reinforcing social bonds in Callicebus and may account for 10% of a day's activity. Group members also twine their tails when sitting together. When aggravated, Pithecia exhibits an aggressive display of piloerection, body shaking, an arched posture, and a growling vocalization. Chiropotes has a distinctive tail wagging behavior that denotes excitement, and a characteristic high-pitched whistling vocalization. Cacajao also exhibits tail wagging and piloerection, and the naked-faced Cacajao calvus has the largest repertoire of facial expressions of any platyrrhine.
Callicebus lives in small, well-defined territories that in most species are defended using loud vocalizations (solo male calls and male-female duets). In other species there is overlap of home ranges, and calls are used to define territories without boundary defense. They rarely associate with other primate species, but have been observed occasionally with tamarins (genus Saguinus) and marmosets (genus Callithix). Pithecia generally occupies small home ranges, but some species may have large ones. The home ranges of some species may overlap, while others may have relatively exclusive areas with defined boundaries and little overlap. They have not been observed to form polyspecific associations with other primates. Both Chiropotes and Cacajao have large home ranges that are not defended. Chiropotes has been observed in polyspecific groups with squirrel monkeys (genus Saimiri), capuchin monkeys (genus Cebus), and Cacajao; and Cacajao has been observed to associate with squirrel monkeys (genus Saimiri), capuchin monkeys (genus Cebus), woolly monkeys (genera Lagothrix, Pithecia, and Chiropotes).
Both Pithecia and Chiropotes have relatively shorter day ranges than do the other two pitheciid species. Pithecia has short day ranges, usually less than 0.6 mi (1.0 km). Most Pithecia species locomote by vertical clinging and leaping and tend to prefer the lower and middle strata of the forest canopy, although Pithecia albicans uses the middle and upper canopy and does little vertical clinging. Some species will forage occasionally on the ground. Day ranges are much longer in Chiropotes (0.6–2.8 mi [1.0–4.5 km]), and increase during periods of food scarcity. Groups may fission for feeding. Travel is cohesive but they may also travel in subgroups. Chiropotes is an arboreal quadruped that prefers the upper canopy, traveling rapidly between feeding trees and then engaging in intense feeding bouts. Cacajao also has very long day ranges (greater than 3 mi [5 km]), and prefers the middle and upper canopy, but will forage on the ground during the dry season due to the paucity of terrestrial mammals in flooded forests. They are arboreal quadrupeds, but employ more leaping and bipedal suspension postures than other pitheciids. All Callicebus species are primarily arboreal quadrupeds and rarely forage on the ground. Some species use the lower canopy, some the middle canopy, and some others the upper canopy.
Feeding ecology and diet
The three pitheciin genera, and to a lesser extent Callicebus, are specialized seed predators. Pithecia, Chiropotes, and Cacajao all include a large percentage of fruit in their diets, and the majority of these fruit are exploited for the seeds they contain. Most species prefer young seeds from unripe fruit. The fruits these primates include in their diets are primarily large, hard, indehiscent fruits with one or a few large seeds, such as the Brazil nut family (Lecythidaceae). Pithecia supplements its diet with leaves, flowers, and invertebates, as does Cacajao. Chiropotes eats fewer leaves, but will eat some invertebrates. Callicebus species eat more fruit pulp and fewer seeds than other pitheciids. Some species supplement their diet with insects while others eat leaves.
Reproductive biology
Saki (Pithecia) reproductive biology is variable. All species give birth to single offspring. Some species (P. pithecia and P. monachus) reproduce seasonally, while others (P. albicans) do not. Groups may have a single reproductive female (P. monachus) or more than one (P. pithecia). Adult coloration may develop in weeks (P. albicans), months (P. pithecia), or years (P. monachus). There is typically no paternal care, although fathers may groom infants. In some species, subadult and adult daughters may help. Offspring are independent at 6–7 months and are weaned at one year of age.
Chiropotes satanas gives birth in the dry season in Suriname and Venezuela. There are occasional copulations year-round with a peak from July to September, and gestation is 4.5–5.5 months. By two months, infants are carried ventrally, but begin a shift to dorsal carrying. Other group members groom infants. At three months, infants are always carried dorsally, and they exhibit some self-locomotion at rest. At six months, infants locomote independently for short distances, but are still carried dorsally for long trips. Infants are fully independent at 10–13 months. Chiropotes albinasus does not breed seasonally, but may give birth in February-March or August-September. Adult females exhibit bright red labia during estrus.
In captivity, Cacajao mates promiscuously and has seasonal births of single offspring. Females show no external sign of estrus, and gestation length is unknown. Only mothers carry offspring, and infants are carried ventrally for three months, and then are carried dorsally. At 12 months, infants independently locomote but may still sleep with the mother. Suckling and sleeping on proximity to the mother may last two years. The birth season for wild Cacajao in Peru is December to March.
Callicebus also breeds seasonally and gives birth to a single offspring. These monkeys are unique among pitheciids in that males provide nearly all of the infant care. Male titis begin carrying infants within 48 hours of birth, and infants return to the mother only to nurse. Infants are carried until 4–6 months of age, and weaning occurs at this time. Offspring reach maturity at 3–4 years, at which time they abruptly leave the natal group. No aggression accompanies the departure.
Conservation status
The IUCN lists Miller's monk saki (Pithecia monachus milleri) as Vulnerable due to habitat loss, fragmented populations, and declining numbers of adults. The Napo monk saki (P. monachus napiensis) is listed as Data Deficient.
The IUCN lists Uta Hick's bearded saki (Chiropotes satanas utahicki) as Vulnerable due to habitat loss and the southern bearded saki (C. satanas satanas) as Endangered due to habitat loss and the fragmenting and decline of population sizes. The white-nosed bearded saki (Chiropotes albinasus) is listed as CITES Appendix I.
Bald uakaris (Cacajao calvus) are generally listed as Vulnerable due to severe hunting in many parts of Peru and Brazil. The IUCN also lists the Ucayali bald uakari (Cacajao calvus ucayalii) as Vulnerable due to a loss of habitat, and lists three other subspecies, the white bald uakari (C. calvus calvus), Novae's bald uakari (C. calvus novaesi), and the red bald uakari (C. calvus rubicundus) as Endangered due to habitat fragmentation and population decline. All Cacajao species are CITES Appendix I.
A number of Callicebus species are also listed by the IUCN. Two species, the northern Bahian blond titi (Callicebus barbarabrownae) and Coimbra's titi (C. coimbrai), are Critically Endangered. Six additional species, Medem's collared titi (C. medemi), the southern Bahian masked titi (C. melanochir), the black fronted titi (C. nigrifrons), the Andean titi (C. oenathe), the ornate titi (C. ornatus), and the masked titi (C. personatus), are considered Vulnerable. One species, the Beni titi (C. olallae), is listed as Data Deficient.
Significance to humans
All pitheciid genera are either hunted for food or captured to be sold locally or exported as pets. Pithecia and Chiropotes are often hunted solely for their long, bushy tails, which are used as dusters.
Species accounts
White-faced sakiBearded saki
Bald uakari
Dusky titi monkey
Collared titi
Masked titi
Resources
Books:Clutton-Brock, T. H., ed. Primate Ecology: Studies of Feeding and Ranging Behavior in Lemurs, Monkeys, and Apes. New York: Academic Press, 1977.
Eisenberg, John F., ed. Mammals of the Neotropics, Volume 1: The Northern Neotropics: Panama, Colombia, Venezuela, Guyana, Suriname, French Guiana. Chicago, IL: University of Chicago Press, 1989. ——, ed. Mammals of the Neotropics, Volume 3: The Central Neotropics: Ecuador, Peru, Bolivia, Brazil. Chicago, IL: University of Chicago Press, 1997.
Emmons, Louise H., and Francois Feer. Neotropical Rainforest Mammals: A Field Guide, 2nd ed. Chicago, IL: University of Chicago Press, 1997.
Fleagle, John G. Primate Adaptation and Evolution, 2nd ed. San Diego, CA: Academic Press, 1999.
Groves, Colin P. Primate Taxonomy. Washington, D.C.: Smithsonian Institution Press, 2001.
Hartwig, Walter Carl, ed. The Primate Fossil Record. New York: Cambridge University Press, 2002.
Kinzey, Warren G., ed. New World Primates: Ecology, Evolution, and Behavior. New York: Aldine de Gruyter, 1997.
Norconk, Marilyn A., Alfred L. Rosenberger, and Paul A. Garber, eds. Adaptive Radiations of Neotropical Primates. New York: Plenum Press, 1996.
Peetz, Angela Ecology and Social Organization of the Bearded Saki Chiropotes Satanas Chiropotes (Primates: Pitheciinae) in Venezuela. Bonn, Germany: Society of Tropical Ecology, 2001.
Rowe, Noel. The Pictorial Guide to the Living Primates. East Hampton, NY: Pogonias Press, 1996.
Sussman, Robert W. Primate Ecology and Social Structure, Volume 2: New World Monkeys Needham Heights, MA: Pearson Custom Pub., 1999.
Periodicals:Ayres, J. M. "Comparative Feeding Ecology of the Uakari and Bearded Saki, Cacajao and Chiropotes." Journal of Human Evolution 18 (1989): 697-716.
Barnett, A. A., and D. Brandon-Jones. "The Ecology, Biogeography, and Conservation of the Uakaris, Cacajao (Pitheciinae)." Folia Primatologica 68 (1997): 223-235.
Boubli, J. P. "Feeding Ecology of Black-Headed Uakaris (Cacajao melanocephalus melanocephalus) in Pico Da Neblina National Park, Brazil." International Journal of Primatology 20 (1999): 719-749.
Brush, J. A., and M. A. Norconk. "Early Behavioral Development in a Wild White-Faced Saki Monkey (Pithecia pithecia)." American Journal of Physical Anthropology Suppl. 28 (1999): 99.
Easley, S. P., and W. G. Kinzey. "Territorial Shift in the Yellow-Handed Titi Monkey (Callicebus torquatus)." American Journal of Primatology 11(1986): 307-318.
Ferrari, S. F. "Observations on Chiropotes albinasus from the Rio Dos Marmelos, Amazonas, Brazil." Primates 36 (1995): 289-293.
Happel, R. E. "Ecology of Pithecia hirsuta in Peru." Journal of Human Evolution 11 (1982): 581-590.
Hershkovitz, P. "A Preliminary Taxonomic Review of the South American Bearded Saki Monkeys Genus Chiropotes (Cebidae, Platyrrhini), with the Description of a New Subspecies." Fieldiana Zoology 27 (1985): 1-46. ——. "Uacaries, New World Monkeys of the Genus Cacajao (Cebidae, Platyrrhini): A Preliminary Taxonomic Review with the Description of a New Subspecies." American Journal of Primatology 12 (1987): 1-53. ——. "The Taxonomy of South American Sakis, Genus Pithecia (Cebidae, Platyrrhini): A Preliminary Report and Critical Review with the Description of a New Species and a New Subspecies." American Journal of Primatology 12 (1987): 387-468.
Kinzey, W. "Dietary and Dental Adaptations in the Pitheciinae." American Journal of Physical Anthropology 88 (1992): 499-514.
Kinzey, W. G., and M. Becker. "Activity Pattern of the Masked Titi Monkey, Callicebus personatus." Primates 24 (1983): 337-343.
Kinzey, W. G., and M. A. Norconk. "Hardness as a Basis of Fruit Choice in Two Sympatric Primates." American Journal of Physical Anthropology 81(1990): 5-15. ——. "Physical and Chemical Properties of Fruit and Seeds Eaten by Pithecia and Chiropotes in Surinam and Venezuela." International Journal of Primatology 14 (1993): 207-227.
Kinzey, W. G., and J. G. Robinson. "Intergroup Loud Calls, Range Size, and Spacing in Callicebus torquatus." American Journal of Physical Anthropology 60(1983): 539-544.
Kinzey, W. G., A. L. Rosenberger, P. S. Heisler, D. L. Prowse, and J. S. Trilling. "A Preliminary Field Investigation of the Yellow Handed Titi Monkey, Callicebus torquatus torquatus, in Northern Peru." Primates 18 (1977): 159-181.
Kinzey, W. G., and P. C. Wright. "Grooming Behavior in the Titi Monkey (Callicebus torquatus)." American Journal of Primatology 3 (1982): 267-275.
Lehman, S., W. Prince, and M. Mayor. "Variations in Group Size in White-Faced Sakis (Pithecia pithecia): Evidence for Monogamy or Seasonal Congregations." Neotropical Primates 9 (2001): 96-101.
Mittermeier, R. A., and M. G. M. van Roosmalen. "Preliminary Observations on Habitat Utilization and Diet in Eight Surinam Monkeys." Folia Primatologica 36 (1981): 1-39.
Mittermeier, R. A., W. R. Konstant, H. Ginsberg, M. G. M. van Roosmalen, and E. Cordeiro da Silva Jr. "Further Evidence of Insect Consumption in the Bearded Saki Monkey, Chiropotes satanas chiropotes." Primates 24 (1983): 602-605.
Norconk, M. A., C. Wertis, and W. G. Kinzey. "Seed Predation by Monkeys and Macaws in Eastern Venezuela: Preliminary Findings." Primates 38 (1997): 177-184.
Rylands, A. B., H. Schneider, A. Langguth, R. A. Mittermeier, C. P. Groves, and E. Rodriguez-Luna. "An Assessment of the Diversity of New World Primates." Neotropical Primates 8 (2000): 61-93.
Setz, E. Z. F., and D. D. Gaspar. "Scent-Marking Behaviour in Free-Ranging Golden-Faced Saki Monkeys, Pithecia pithecia chrysocephala: Sex Differences and Context." Journal of Zoology 241 (1997): 603-611. van Roosmalen, M. G. M., R. A. Mittermeier, and J. G. Fleagle. "Diet of the Northern Bearded Saki (Chiropotes satanas chiropotes): A Neotropical Seed Predator." American Journal of Primatology 14 (1988): 11-35.
Walker, S. E., and J. M. Ayres. "Positional Behavior of the White Uakari (Cacajao calvus calvus)." American Journal of Physical Anthropology 101 (1996): 161-172.
Organizations
Conservation International. 1919 M Street, NW, Suite 600, Washington, DC 20036 United States. Phone: (202) 912-1000; 1 (800) 406-2306. Web site:
Primate Center Library, Wisconsin Primate Research Center. 1200 Capitol Court, Madison, WI 53715-1299 United States. Phone: (608) 263-3512. Fax: (608) 263-4031. E-mail: library@primate.wisc.edu Web site:
World Wildlife Federation (WWF)—The Conservation Organization. 1250 24th Street NW, Washington, DC 20037-1193 United States. Phone: (202) 293-4800. Fax: (202) 293-9211. Web site:
[Article by: Brian W. Grafton, PhD]
