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Red Titi (Callicebus cupreus)


MORPHOLOGY:
The tail of this species is not prehensile but does serve a balancing function when locomoting (Kinzey, 1981). The dental formula is 2:1:3:3 on both the upper and lower jaws (Ankel-Simons, 2000). The first two lower molars have relatively long shearing crests that is an adaptation of having leaves in the diet (Kinzey and Gentry, 1979). In this species the hindlimbs are relatively shorter than the forelimbs (Ankel-Simons, 2000). The average body mass for this species ranges from 1200-1500 grams (Aquino and Encarnacion, 1994).

This species has three subspecies, each having a different pelage coloration:
  • Callicebus cupreus cupreus: The ventral side, sideburns, and legs are reddish in color (Hershkovitz, 1990). The upper and outer sides of the trunk and the crown are buffy agouti in color (Hershkovitz, 1990). The forehead has the same coloration as the crown except for some blackish fringe (Hershkovitz, 1990).
  • Callicebus cupreus discolor: The forehead has a whitish or buffy colored tuft that contrasts with the agouti colored region of the anterior crown (Hershkovitz, 1990). The sideburns, side of the neck, lower arms, legs, chest, and belly are reddish in color (Hershkovitz, 1990). The crown, sides of body, back, and tail of this subspecies are agouti in color (Hershkovitz, 1990). The terminal third of the tail is predominately buffy in color (Hershkovitz, 1990).
  • Callicebus cupreus ornatus: On the forehead there is a pale frontal blaze, a pale strip across the forehead (Hershkovitz, 1990). The crown is colored reddish brown to nearly blackish with the base of the hairs whitish or buffy (Hershkovitz, 1990). The sideburns, ventral side, inner side of limbs, outer side of legs, and lower part of forearms are reddish in coloration (Hershkovitz, 1990). The digits are pale contrasting with that of the lower forearms (Hershkovitz, 1990). The outer side of the thighs and the upper arms are buffy agouti in color in this subspecies (Hershkovitz, 1990).
Red Titi


RANGE:
This species is found in the countries of Brazil, Colombia, Ecuador and Peru. The red titi in Colombia is found in gallery forests and isolated patches of woods (Kinzey, 1981). This species occurs where lianas are frequent and in bamboo thickets (Kinzey, 1981).

The three subspecies of this species each have distinct ranges:

ECOLOGY:
The red titi is a frugivorous species (Kinzey, 1981). Fruits eaten are generally of the soft type (Kinzey, 1978). Figs, Ficus, are an important fruit species consumed by the red titi (Kinzey and Gentry, 1979). This species also incorporates leaves into the diet (Kinzey, 1981). A captive member of the subspecies Callicebus cupreus ornatus that escaped in Louisiana, U.S.A., consumed leaves, fruits, flowers, pollen, insect wings (Odonata and Orthoptera), and acorns (Quercus) (Jones et al., 1970; cited in Kinzey, 1981). Members of a group feed upon the same food items at the same time (Kinzey et al., 1977; cited in Kinzey, 1981). This species forages in the lower levels of the canopy of the forest (Rowe, 1996). This species feeds intensively in the early morning, then takes about an hour rest during the mid-day, then resumes feeding (Kinzey, 1981, 1978). In the two hours before sleeping for the night, group members will forage upon leaves intensively (Kinzey, 1981).

The red titi is a diurnal and an arboreal species that rarely comes to the ground (Kinzey, 1981). Group sizes for the red titi range from 2 to 4 individuals (Kinzey, 1981). For the subspecies Callicebus cupreus ornatus the group size was found to range from 1 to 5 individuals (Polanco-Ochoa and Cadena, 1993). Groups will begin daily activity at the first hint of dawn, which first includes urination and defecation followed by calling that includes moaning (Mason, 1966; Robinson, 1979). After calling the group will leave the sleeping site and move towards feeding areas where they will feed primarily on fruits and berries (Mason, 1966). During feeding the group will frequently encounter other groups also feeding nearby (Mason, 1966). The activities of this species mostly take place in the lower to middle levels of the forest (Aquino and Encarnacion, 1994). This species spends from 60 to more than 90% of the time resting (Kinzey, 1981). During daily travel, the group will follow the same path day after day, returning to the same locations (Menzel, 1986). The subspecies Callicebus cupreus ornatus was found to have the following forests types in its home range: mature and intermediate forests, vine thickets, and flood forests (Polanco-Ochoa and Cadena, 1993). The core area of this subspecies was found to mostly contain a vine thicket type of forest, and this area was utilized more than 50% of the time (Polanco-Ochoa and Cadena, 1993). The subspecies Callicebus cupreus ornatus prefers to utilize types of forest with branches that are horizontal and thin (2 to 10 centimeters in diameter) (Polanco-Ochoa and Cadena, 1993). The subspecies Callicebus cupreus discolor was observed to sleep in trees in areas with a large number of palms, lianas, and dense undergrowth (Kinzey, 1981). The subspecies Callicebus cupreus ornatus has also been observed to sleep in trees with dense foliage (Robinson, 1977; cited in Kinzey, 1981). Callicebus cupreus ornatus was also observed to sleep in vine thicket type forest on branches that were about 10 centimeters in diameter and 15-20 meters in height, with the trees being from 20-25 meters tall (Polanco-Ochoa and Cadena, 1993). Red titis will sleep together in a huddle with the tails entwined (Robinson, 1979).

LOCOMOTION:
The red titi moves through the understory of the forest quadrupedally as well as by, although to a lesser degree, leaping (Fleagle, 1988). This species moves along the upper surfaces of supports (Kinzey, 1981; Yoneda, 1988). The red titi prefers to utilize trees with a height range from 0-5 meters (Yoneda, 1988).

SOCIAL BEHAVIOR:
The red titi has a monogamous mating system and mates for life. A strong bond exists between the male and female of a pair, with the pair spending much time huddling, tail-entwining, and grooming (Anzenberger et al., 1986; Mason, 1974; Mason, 1966; Fernandez-Duque et al., 1997). Although extra-pair copulations between neighboring members of a pair have been noted in the wild (Mason, 1966). Separation from a pair caused increases in emotional arousal, which include higher rates of locomotion, high-pitched vocalizations, and heart rate (Cubicciotti and Mason, 1975). In captivity it was found that pairs of this species have more closely coordinated activities than pairs of the genus Saimiri (Mason, 1974). Red titi pairs also engage in more contact than members of the genus Saimiri (Mason, 1974). Pairs of red titis were tested in captivity to see whether they preferred their partner or a strange conspecific, and it was found that both males and females preferred their mates over opposite sex conspecifics (Mason, 1975). When members of a pair are separated and then reunited, there is an increasing in the amount of grooming between the pairs (Fernandez-Duque et al., 1997). Males were found to show jealous behavior when their mate was placed with a conspecific male in captivity (Cubicciotti and Mason, 1978). Both males and females of the red titi disperse from their natal groups (Valeggia et al., 1999). The stimulus for this dispersal lies not in the aggression of the parents towards the young, but rather in a developmental changes in young that may be associated with an attraction to strange conspecifics (Mason et al., 1994; Mayeaux and Mason, 1994). Mason (1966) noted that separation between young adults and parents occurs slowly over time. Teskey et al. (1993) found that although parents are responsive to stimuli produced by infants, they do not necessarily show an attachment to their own infants. This species has been observed to form mixed-species groups with Saguinus fuscicollis, but this behavior is described as being rare (Kinzey, 1981). A dominance hierarchy doesn’t seem to exist (Kinzey, 1997). The basic group is composed of the breeding pair and their offspring. Grooming is an important activity that serves to strengthen social bonds amongst members of the group.

This species, like members of the genus Callicebus, is highly territorial (Kinzey, 1997; Mason, 1966). The territory for this species is almost exclusive (Robinson, 1979). Encounters between pairs of adjacent territories are common (Anzenberger et al., 1986). When pairs encounter each other duetting occurs (Anzenberger et al., 1986). Males will respond more vigorously to confrontations with other pairs (Anzenberger et al., 1986). Duetting also is known to stimulate other pairs to approach the territory of the pair that is duetting (Robinson, 1981). Duetting also has the function of keeping other conspecifics from a pair's mate, extra-pair copulations have been noted to occur (Robinson, 1981; Mason, 1966). At territorial boundaries, individuals tend to moan more (Robinson, 1981). During territorial encounters the opposing pairs will stand and face each other (Mason, 1966). Sometimes individual leap towards a member of the other pair, and this behavior may result in chasing (Mason, 1966). Chest-rubbing has also been noted to occur during territorial encounters by pairs (Mason, 1966). The rubbing may occur either along a branch or the hands may be rubbed against the chest with slow, downward movements (Mason, 1966).

The males participate in caring for the infants. Males start to carry infants about 48 hours after birth, and the males become the primary carriers, and carrying is most often done dorsally (Kinzey, 1981; Fragaszy et al., 1982; Hoffman et al., 1995; Jantschke et al., 1995; Jantschke and Welker, 1996; Mendoza and Mason, 1986). Fathers were found to carry the infants for 85.3% of the time (Mendoza and Mason, 1986). Infants were found to spend more time in proximity with fathers than with mothers (Hoffman et al., 1995). In captivity Hoffman et al. (1995) found that removal of the fathers brought on greater stress to the infant than removal of the mothers. Fathers were found in captivity to retrieve infants in distress more than females and older juveniles; males tend to retrieve infants when they are fathers as opposed to when the infant is a sibling (Mason and Mendoza, 1998). Infants of this species begin to move around on their own starting between 2.5 and 3.5 months, but the males still stay close to the infants (Kinzey, 1981). When the infant wishes to nurse, the male will sit close to the female and the infant either climbs on its own to the female or the female will remove the infant from the male, lick the genitals, and then place the infant on her ventrum (Kinzey, 1981). When done with nursing the infant either climbs back on to the male or is removed by the male (Kinzey, 1981). Punitive behaviors (punishment) were found only to be given to the infants by the mothers and this usually occurred when the mother attempted to remove a clinging infant (Mendoza and Mason, 1986). In captivity infants were observed to be in contact, clinging, with all members of the family group (Fragaszy et al., 1982). Newborns would first cling to the carrier's neck before switching to a parallel dorsal posture that is typical of older infants (Fragaszy et al., 1982). Infants have been found to groom their fathers but not any other group members (Jantschke et al., 1995). Infants at about the ages 4-5 months spend more time sitting next to rather than on a carrier, and between 3-4 months of age fathers will start to resist the clinging of the infants (Fragaszy et al., 1982). Young are however still found be carried up to 6 months of age (Jantschke et al., 1995). Young females have been found in captivity to be more inclined to explore their social surroundings (Hoffman et al., 1997). Although fathers carry the infants more than the mothers, it was found in captivity that both mates, including the father, preferred their own mate over their own infant (Mendoza and Mason, 1986).

Social play in the red titi usually occurs between the juvenile and the adult male (Kinzey, 1981). Play often occurs between the adult male and juvenile when they are engaging in social grooming, and the juvenile would grab the tail of the adult male (Kinzey, 1981). Infants have also been observed to play with older siblings, this included chasing, parallel running, batting one another, and gentle biting of the hands (Fragaszy et al., 1982). Fragaszy et al. (1982) found that social play was more common between infants and older siblings than between infants/juveniles and adult males.

VOCAL COMMUNICATION:
chirps: This call is described as being a pure tone at a frequency of 6 kilohertz (Kinzey, 1981). This call occurs while foraging (Kinzey, 1981).

grunts: This call is described as being a short burst having energy up to 3 kilohertz (Kinzey, 1981). This call occurs before and after duetting (Kinzey, 1981).

sneezes: This call is described as being a short noisy burst having a frequency as high as 8 kilohertz (Kinzey, 1981). This call occurs when an individual is disturbed (Kinzey, 1981). This call is accompanied by lateral movements of the head (Moynihan, 1966). This call may be accompanied by escape intention movements (Moynihan, 1966).

infant distress call: This call is described as being a faint buzz (Kinzey, 1981). This occurs when an infant is disturbed and off of the father's back (Kinzey, 1981). The father will approach the infant and allow it to climb on it's back (Kinzey, 1981).

chirrups: This call is produced by inhalation and the pitch of this call differs by age and sex class (Kinzey, 1981). This call is heard when locating and recognizing group members (Kinzey, 1981). This serves to enforce group cohesion (Kinzey, 1981).

chuck notes: This call is very sharp, short, relatively loud, and sounds like "chuk" (Moynihan, 1966). This call is common in hostile situations (Moynihan, 1966). This call is followed vigorous attack or escape movements (Moynihan, 1966).

moans: This call is produce by only adults and there are differences of this call between the sexes (Kinzey, 1981). This is heard during situations of disturbances by other animals, including primates (Kinzey, 1981). This call may be a prelude to duetting and the mate approaches the moaning individual (Kinzey, 1981). This behavior keeps the group pair in proximity (Robinson, 1981).

pants: This call is given in phrases as part of a longer sequence of calls (Kinzey, 1981). There is a sex difference in this call (Kinzey, 1981). This call occurs during male and female calling and during duetting (Kinzey, 1981).

honks: This call is lower in intensity than pants and may be given by either the males or females (Kinzey, 1981). This call is always part of a longer sequence (Kinzey, 1981).

bellows: This is the loudest call the red titi can make and there is differences between the sexes (Kinzey, 1981). This call is heard during male and female calling and during duetting (Kinzey, 1981). This call is used to maintain distances between neighboring groups (Robinson, 1979).

pumps: This call has the characteristics of being rapidly descending in pitch with a short climax (Kinzey, 1981). There is a difference between the sexes in this call (Kinzey, 1981). This call occurs in nearly all sequences (Kinzey, 1981).

screams: This call has two syllables which is an inhale followed by an exhale (Kinzey, 1981). This is heard during fighting between young males in this species (Kinzey, 1981). This call may begin and/or end with a loud or sharp sound (Moynihan, 1966).

squeaks: This call is very short and made up of soft notes (Moynihan, 1966). This vocalization may be either uniform in pitch, steeply ascending, or steeply descending (Moynihan, 1966). This call may precede and/or accompany low intensity escape movements (Moynihan, 1966).

whistles: This call is similar to squeaks in terms of loudness and in pitch (Moynihan, 1966). This call rises and falls in pitch repeatedly (Moynihan, 1966). This call is uttered during intra-specific disputes and during fights (Moynihan, 1966). This call is also heard during vigorous social grooming bouts, vigorous play wrestling, and females resisting unwelcome copulation attempts (Moynihan, 1966). When an individual is lost (separated from their companion) they may emit this call (Moynihan, 1966).

trills: This is a rapid series of short notes repeated one right after another (Moynihan, 1966). This call resembles a single, short squeak (Moynihan, 1966). This call is uttered during intra-specific disputes and during fights (Moynihan, 1966). This call is also heard during vigorous social grooming bouts, vigorous play wrestling, and females resisting unwelcome copulation attempts (Moynihan, 1966). When an individual is lost (separated from their companion) they may emit this call (Moynihan, 1966).

OLFACTORY COMMUNICATION:
social sniffing: This is when one individual will sniff another's face or other body part (Kinzey, 1981). This behavior occurs when unfamiliar individuals are brought together and this is a reciprocal behavior (Kinzey, 1981). Adult males will sniff the genital or perineal region of a female they are mated with (Moynihan, 1966).

chest-rubbing: This is when the chest is rubbed along a branch (Kinzey, 1981). This behavior is described as being sporadic (Kinzey, 1981). This is done by males and may be used to demarcate the territory (Moynihan, 1966).

VISUAL COMMUNICATION:
displacement-scratch: This is when an individual will vigorously scratch the chest (Kinzey, 1981). This is a displacement behavior (Kinzey, 1981).

protruding-lips: This is when an individual will protrude the lips forward. This display may be accompanied by moans or resonating notes (Kinzey, 1981). This behavior communicates weak excitement (Kinzey, 1981).

arch-posture: This is when an individual has the back raised with a strong curve (Kinzey, 1981). This behavior may be followed by attack or escape (Kinzey, 1981). This behavior is very common (Kinzey, 1981).

tail-raising: This is when an individual raises the tail (Kinzey, 1981). This behavior communicates hostility (Kinzey, 1981).

tail-lashing: This when an individual will swing the tail from side-to-side (Kinzey, 1981). This behavior is seen during hostile encounters (Kinzey, 1981). This is responded to by calling from the opposing group (Kinzey, 1981).

piloerection: This is when the hairs are erected (raised) on the body, limb, and tail (Kinzey, 1981). This behavior shows hostility and often occurs with arch-posture (Kinzey, 1981).

TACTILE COMMUNICATION:
social grooming: This is when individual removes parasites or dead skin from another individual. This behavior is frequent during rest periods (Kinzey, 1981). This behavior is common between adult males and females and between adult males and the youngest member of the group (infants/juveniles) (Kinzey, 1981). However, Hoffman et al. (1995) found there was no difference between grooming occurring between adult males and infants and adult females and infants. This behavior is reciprocal (Kinzey, 1981).

tail-entwining: This is used to reinforce bonds amongst pairs. This is where two individuals are sitting and have their tails wrapped around each other's. This behavior is sporadic during the day and occurs during sleeping (Kinzey, 1981). This behavior also helps the red titi balance themselves (Moynihan, 1966).

REPRODUCTION:
The red titi gives birth to a single offspring. Twins have been reported to occur in captivity and in the wild, but usually one infant dies within a few days of birth (Valeggia et al., 1999; Knogge and Heymann, 1995). The average gestation length for the red titi is 128.6 days (Valeggia et al., 1999). The birth season for this species is between November and March (Kinzey, 1981). Valeggia et al. (1999) found a birth peak between December and March, but noted that births could occur throughout the year. Red titis have a body mass of about 100 grams at birth (Fragaszy et al., 1982). the average interbirth interval for this species is 335.5 days (Valeggia et al., 1999). This interbirth interval shrinks when the female has an infant die within the first week, then the average interbirth interval is 249.6 days (Valeggia et al., 1999). Jantschke et al. (1995) found the average interbirth interval to be 318 days. Mature females living with their parents will not become pregnant, even though they are capable of becoming pregnant, showing there may be social suppression of reproduction in this species (Valeggia et al., 1999).

REFERENCES:
Ankel-Simons, F. 2000. Primate Anatomy: An Introduction. Academic Press: San Diego.

Anzenberger, G., Mendoza, S.P., and Mason, W.A. 1986. Comparative studies of social behavior in Callicebus and Saimiri: Behavioral and physiological responses of established pairs to unfamiliar pairs. American Journal of Primatology. Vol. 11, 37-51.

Aquino, R. and Encarnacion, F. 1994. Primates of Peru. Primate Report. Vol. 40, 1-127.

Cubicciotti, D.D. and Mason, W.A. 1975. Comparative studies of social behavior in Callicebus and Saimiri: Male-female emotional attachments. Behavioral Biology. Vol. 16, 185-197.

Cubicciotti, D.D. and Mason, W.A. 1978. Comparative studies of social behavior in Callicebus and Saimiri: Heterosexual jealousy behavior. Behavioral Ecology and Sociobiology. Vol. 3, 311-322.

de la Torre, S., Utreras, V., and Campos, F. An overview of primatological studies in Ecuador: Primates of the Cuyabeno Reserve. Neotropical Primates. Vol. 3(4), 169-171.

Fernandez-Duque, E., Mason, W.A., and Mendoza, S.P. 1997. Effects of duration of separation on responses to mates and strangers in the monogamous titi monkey (Callicebus moloch). American Journal of Primatology. Vol. 43, 225-237.

Fleagle, J. G. 1988. Primate Adaptation and Evolution. Academic Press: New York.

Fragaszy, D.M., Schwartz, S., and Shimosaka, D. 1982. Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch). American Journal of Primatology. Vol. 2, 191-200.

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Hoffman, K.A., Mendoza, S.P., Hennessy, M.B., and Mason, W.A. 1995. Responses of infant titi monkeys, Callicebus moloch, to removal of one or both parents: Evidence for paternal attachment. Developmental Psychobiology. Vol. 28(7), 399-407.

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Kinzey, W.G., Rosenberger, A.L., Heisler, P.S., Prowse, D., and Trilling, J. 1977. A preliminary field investigation of the yellow handed titi monkey, Callicebus torquatus torquatus, in northern Peru. Primates. Vol. 18, 159-181.

Knogge, C. and Heymann, E.W. 1995. Field observation of twinning in the dusky titi monkey, Callicebus cupreus. Folia Primatologica. Vol. 65, 118-120.

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Rowe, N. 1996. The Pictorial Guide to the Living Primates. Pogonias Press: East Hampton, New York.

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Valeggia, C.R., Mendoza, S.P., Fernandez-Duque, E., Mason, W.A., and Lasley, B. 1999. Reproductive biology of female titi monkeys (Callicebus moloch) in captivity. American Journal of Primatology. Vol. 47, 183-195.

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Last Updated: October 5, 2003.
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