Collared Titi (Callicebus torquatus)



MORPHOLOGY:
The average body mass for the adult male is 1490.8 grams and for the adult female it is 1265.1 grams (Hernandez and Defler, 1985). The tail of the collared titi is not prehensile. The dental formula is 2:1:3:3 on both the upper and lower jaws (Ankel-Simons, 2000). The male canines are 3-4% larger than the females canines (Kinzey, 1972; cited in Kinzey, 1981).

This species has six subspecies each having their own pelage coloration:

RANGE:
The collared titi is found in the countries of Brazil, Colombia, Ecuador, Peru, and Venezuela. This species lives in mixed, gallery, and evergreen forests located near streams. This species is restricted to areas where plants grow on white sand soils (Kinzey and Gentry, 1979). A recent study, however, found that this is not true and that this species inhabits forests that are mostly on clay-soils rather than white sand (Defler, 1994). In Colombia this species tends to prefer to live in well-drained, upland forests, that grow on a variety of soils (Defler, 1994).

This species has six subspecies each having their own range:

ECOLOGY:
The collared titi is primarily a frugivorous species, but also eats leaves and insects. The diet of this species is 74% fruits, 25.8% insects, 8.8% leaves, and 0.6% flowers and buds (Easley, 1982; cited in Palacios et al., 1997). The subspecies Callicebus torquatus lucifer was found to have a diet that included 37% seeds, 30% fruit, 13% leaves, and 14% insects (Kinzey, 1977; cited in Kinzey, 1992). The collared titi will us its incisors to scrape off the mesocarp of palm fruits like Jessenia bataua (Kinzey, 1992). On of the more important fruits items consumed is the ungurahui palm, Jessenia polycarpa (Kinzey et al., 1977). Fruits eaten tend to be relatively hard (Kinzey, 1978). This species obtains most of its protein from insects (Kinzey, 1978). The collared titi feeds in emergent trees with large crown diameters this because of the low amount of other primate species for competition (Kinzey, 1977). This species feeds on immature seeds when there is a lack of available fruit (Palacios et al., 1997). The subspecies Callicebus torquatus lugens may not include insects in the diet at the end of the rainy season/beginning of the dry season (Milton and Nessimian, 1984). This species will not feed in the same tree where other primate species are feeding (Kinzey, 1992). For the subspecies Callicebus torquatus lucifer feeding takes place mostly (51%) in the varillal alto seco vegetational zone, with palmal (28%) being the second most popular (Kinzey, 1976). Most feeding for the subspecies Callicebus torquatus lucifer occurs on terminal branches (Kinzey, 1976).

A study on the subspecies Callicebus torquatus lugens found that the diet consisted of 59.4% fruits, 26.9% immature seeds, 6.4% leaves, leaf buds, liana tips, and stems, 3.9% flowers, and 3.4% insects and spiders (Palacios et al., 1997). Feeding on fruits includes mature arils, mesocarps, and pericarps (Palacios et al., 1997). Seeds had the highest rate of consumption in the month of October (Palacios et al., 1997). The species most commonly consumed of its seeds was Sandwithia heterocalyx (Palacios et al., 1997). This subspecies chooses to consume more easily-to-open seeds because of the lack of special dental apparatus (Palacios et al., 1997). The vegetative matter consumed included 38.3% mature leaves, 33% leaf buds, 20% new leaves, 6.7% liana tips, and 2% stems (Palacios et al., 1997). Feeding on flowers were from two species, Anaxagorea brachycarpa (Annonaceae) and Heterostemon conjugatus (Caesalpiniaceae), with 90% of the feeding on Heterostemon conjugatus (Palacios et al., 1997). Insect feeding was mostly on ants, especially two species, Cephalotes atratus and Ectatomma tuberculatum (Palacios et al., 1997). This subspecies was also found to consume coleopterans, orthopterans, hymenopterans, and pupae (Palacios et al., 1997). This subspecies was found to feed mainly in the core area of the home range, defending certain food trees from other conspecific groups (Palacios et al., 1997). This subspecies will consume more immature seeds when over foods are scarce (Palacios et al., 1997).

A study on the subspecies Callicebus torquatus lucifer found that the diet is composed of 67% fruits, 14% insects, 13% leaves, and 6% unknown (Kinzey, 1977). The fruits consumed included 25% nuts, 24% liana nuts, 15% palm fruits, 12% drupes and pomes, 10% berries, 8% gelatinous arilloids, and 6% seeds (Kinzey, 1977). Examples of fruit eaten include Jessenia polycarpa, Clarisia sp., Brosimum sp., Cordia sp., Rheedia sp., Tovomita sp., Maripa spp., Virola sp., Machaerium sp., Coccoloba sp., Pithecolobium sp., and Psychotria axilaris (Kinzey, 1977). Most of the leaves consumed were immature and new growth at the tips of lianas and leaf petioles were also eaten (Kinzey, 1977). Insects consumed by this subspecies include ant nests, insect galls, small flying insects grabbed from the air, beetles, and hymenopteran larva (Kinzey, 1977). This subspecies has on average 3.5 major feeding bouts per day (Kinzey, 1977). Most feeding occurred in the second level of the canopy at a height range from 15 to 25 meters (Kinzey, 1977). Most feeding for this subspecies was done in the varillal alto seco vegetational zone (Kinzey, 1977). Berries, however, were most often eaten in the varillal bajo seco vegetational zone, seeds in the varillal alto humido, gelatinous arilloids in the palmal, and liana nuts in the palmal (Kinzey, 1977).

When feeding on a vertical support the thin trunk is grasped between the hallux and the rest of the toes and one hand grasps the trunk while the other is free for foraging (Kinzey, 1976). When feeding on terminal supports an individual will have one foot grasping one branch and the other foot grasping a branch that forks away from the former (Kinzey, 1976). All toes but the hallux (big toe) are used in grasping and one hand usually grasps a branch while the other is free for foraging (Kinzey, 1976). The tail is usually draped over a neighboring branch for added support (Kinzey, 1976). Juveniles have been observed to forage for fruit by hanging by the hind feet and grasping fruit below (Kinzey, 1981).

This species is diurnal and arboreal and rarely comes to the forest floor (Kinzey, 1997). Group sizes for the collared titi generally range from 3 to 4 individuals (Kinzey et al., 1977). The mean group size for the subspecies Callicebus torquatus torquatus in Brazil was found to be 3.4 individuals (Johns, 1986). The home range of this species is reduced during the rainy season (Campos et al., 1992). The collared titi has a home range that is larger on average than the dusky titi, Callicebus moloch (Kinzey, 1976). Ten percent of day activity is social grooming (Kinzey and Wright, 1982). Daily activity begins for this species with the group moving out of the sleeping tree with the adult female the first individual to do so (Kinzey et al., 1977). The first major feeding bout occurs about an hour after dawn (Kinzey et al., 1977). When feeding the adult male and the infant will feed close to each other while the adult female will feed farther away (Kinzey et al., 1977). There is another feeding peak in the late morning then another in the early afternoon (Kinzey et al., 1977). The adult female leads the group in its daily ranging pattern searching out new food sources (Kinzey et al., 1977). The adult male directs the activity of the group (Kinzey et al., 1977). Most of the time this species is in the middle story of the canopy, but when in the upper story the collared titi will most of the time feeding (Kinzey et al., 1977).

The collared titi sleeps out in the open on large, horizontal branches that have an average diameter of 25 centimeters (Kinzey, 1981; Kinzey and Wright, 1982; Kinzey et al., 1977). No sleeping tree is used twice (Kinzey et al., 1977). The sleeping trees were found to have a height ranging from 17-33 meters (Kinzey et al., 1977). The branch for the sleeping site tends to be located above the closed canopy with having other branches above it (Kinzey et al., 1977). Having a sleeping site at this height could allow groups to be better able to scan the area for predators and other groups, and early morning loud calls travel better above the canopy thus making them more easily heard (Kinzey et al., 1977). Sleeping sites occur in both the center and in the periphery of the home range (Kinzey et al., 1977). The subspecies Callicebus torquatus lucifer was found to sleep in trees that were mostly in the varillal alto seco vegetational zone (Kinzey, 1976). Resting also takes place most frequently on horizontal supports, and most often in the lower levels (51%) of the canopy (Kinzey, 1976). The resting posture consists "of an animal sitting with the trunk held horizontal to semierect, both feet grasping the supporting branch and, depending upon size of the branch, the hands grasping or resting on the same branch, a neighboring branch, or held free", with "the tail either hung free or was draped over a neighboring branch" (Kinzey, 1976). The sleeping posture is described as "similar with the trunk hunched in a roughly horizontal position, hands resting on the same support, and tails twined together" and " sometimes the adult male lay prone on a horizontal branch, with all four limbs draped over the side of the support" (Kinzey, 1976).

LOCOMOTION:
The collared titi moves through the understory of the forest quadrupedally as well as by leaping (Fleagle, 1988; Kinzey, 1976). This species often uses vertical clinging when feeding (Fleagle, 1988). Most locomotion occurs on terminal branches (Kinzey et al., 1977; Kinzey, 1976). Leaping from one terminal branch to another mostly occurs in the middle level of the canopy (Kinzey, 1976). Leaping from one vertical support to another is usually associated with feeding on berry bushes in the lower levels of the forest (Kinzey, 1976). For the subspecies Callicebus torquatus lucifer most locomotion takes place in the varillal alto seco vegetational zone (52%), with the palmal (31%) the second most popular (Kinzey, 1976).

SOCIAL BEHAVIOR:
The collared titi has a monogamous mating system and mates for life. A dominance hierarchy does not 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. The males are the primary caregivers of the infants. The male will carry the infant on his back (Kinzey, 1981). After the young has started to locomote on its own, the adult male would still stay in close contact with it (Kinzey, 1981). There may be increased parental care by the adult males because of knowledge of paternity by the male where he can almost be sure the offspring are his (Kinzey et al., 1977). The adult male and infant spend most of the time together with the adult female away for them (Kinzey et al., 1977). The infant and the adult female only come into contact for nursing (Kinzey et al., 1977). Infants and juveniles will beg for food from adult males and infrequently from adult females (Starin, 1978). Begging will entail staring at the individual with the food, and/or placing the hands, face and/or mouth to the mouth, hands, and/or food of the individual with the food (Starin, 1978). Characteristics of food items that are begged for include: large in size, in limited supply, take a long time to consume, and require skill in locating, capturing, processing (Starin, 1978). Examples of fruit begged for include Annona sp. and Dororia longifolia (Starin, 1978). Both males and females disperse from their natal groups at three years of age (Easley and Kinzey, 1986). Dispersal tends to occur two to four months before the birth of an infant (Defler, 1983). A group may shift its territory to allow a dispersing offspring to take over the vacant part of the territory to start a new group (Easley and Kinzey, 1986). A subadult male was found to establish a territory by emitting a large number of short vocalizations from the center of the territory (Campos et al., 1992). This species, like members of its genus, are highly territorial (Kinzey, 1997). When presented with a duet from a neighboring group the adult male and female of the group will respond with a duet (Kinzey and Robinson, 1983; Defler, 1983). Generally groups do not interact at boundaries but rather call at a distance from the boundary (Kinzey and Robinson, 1983; Easley and Kinzey, 1986; Defler, 1983). During the dry season most calls come from the center of the territory, and during the rainy season groups will move more towards the boundaries before emitting calls directed at another conspecific group (Campos et al., 1992). Territorial defense may be greater during the rainy season because the birth season also occurs at this time (Campos et al., 1992). The collared titi forms mixed-species groups with Saguinus fuscicollis (Kinzey et al., 1977). The titis may benefit from this association because the tamarins are noisy and travel in the lower levels attracting attention away from the titis who are quiet and forage in the upper levels (Kinzey et al., 1977).

Play can occur between the infant and the adult male and by the infant alone (Kinzey et al., 1977). Social grooming between the adult male and infant are sometimes interspersed with social play (Kinzey et al., 1977).

VOCAL BEHAVIOR:
chirrups: This call is soft and is uttered in a slow series (Kinzey et al., 1977). This call is produced by inhalation and the pitch of this call differs by age and sex class (Kinzey, 1981). This serves to enforce group cohesion (Kinzey, 1981). This call is emitted at all times of the day and serves to localize other group members (Kinzey et al., 1977).

dawn call: This call begins at dawn and is given by the adult male (Kinzey et al., 1977). The adult male will perform a display when uttering this call where he runs and leaps through the trees (Kinzey et al., 1977). This call is composed of a series of short sequences of noises that are made up of the components chirrup and pumping notes. This call is given by adult males as a territorial call and can be heard for up to one kilometer. This is also called a loud call.

group solidarity calls: This is a hoot call given by males to promote group cohesion (Kinzey et al., 1977).

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).

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).

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).

chest-rubbing: This is when the chest is rubbed along a branch (Kinzey, 1981). This behavior is described as being sporadic (Kinzey, 1981).

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:
tail-entwining: This is used to reinforce bonds amongst pairs. This is where two individuals are sitting and have their tails wrapped around each others.

social grooming: This is where one individual removes dead skin and/or parasites from another individual. This behavior occurs throughout the day with the most bouts occurring after the group arrives at the sleeping site (Kinzey and Wright, 1982). The two peaks in social grooming occur in midmorning between feeding bouts and shortly after the group arrives at the sleeping site (Kinzey and Wright, 1982). Grooming during the day takes place high in the canopy of the forest (Kinzey and Wright, 1982). The adult female of the pair grooms the adult male more than the adult male grooms the adult female (Kinzey and Wright, 1982). The adult male will groom the juveniles more than the adult female (Kinzey and Wright, 1982). It was found that at the sleeping site a grooming session consisted of 28-78 individual bouts of grooming with each bout lasting an average 2 minutes 57 seconds (Kinzey and Wright, 1982). Social grooming tends to occur more in the dry season than in the wet season (Easley, 1982; cited in Kinzey and Wright, 1982). The collared titi will spend 10% of the day grooming (Kinzey and Wright, 1982). This behavior serves to strengthen the pair bond in this species (Kinzey and Wright, 1982). This behavior is also a form of parental investment for the male collared titi (Kinzey and Wright, 1982).

REPRODUCTION:
The collared titi gives birth to a single offspring. The birth season for the subspecies Callicebus torquatus lucifer in Ecuador was found to be from January to February (Campos et al., 1992). The birth season for the subspecies Callicebus torquatus lucifer in Peru was found to be from November to March (Aquino and Encarnacion, 1994; Kinzey, 1981). Defler (1983) reports that the birth season of the subspecies Callicebus torquatus lugens in Colombia occurs only in the month of January.

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

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

Burton, F. 1995. The Multimedia Guide to the Non-human Primates. Prentice-Hall Canada Inc.

Campos, F., de la Torre, S., and de Vries, T. 1992. Territorial behavior and homerange establishment of Callicebus torquatus (Primates: Cebidae) in Amazonian Ecuador. (abstract) XIV th Congress of the International Primatological Society. Strasbourg, France.

Defler, T.R. 1983. Some population characteristics of Callicebus torquatus lugens (Humboldt, 1812) (Primates: Cebidae) in eastern Colombia. Lozania. Vol. 38, 1-9.

Defler, T.R. 1994. Callicebus torquatus is not a white-sand specialist. American Journal of Primatology. Vol. 33, 149-154.

Easley, S.P. 1982. The ecology and behavior of Callicebus torquatus (Cebidae, Primates). Unpublished Ph.D. dissertation, Washington University, St. Louis.

Easley, S.P. and Kinzey, W.G. 1986. Territorial shift in the yellow-handed titi monkey (Callicebus torquatus). American Journal of Primatology. Vol. 11, 307-318.

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Hernandez-C.J. and Defler, T.R. 1985. Some aspects of the conservation of non-human primates in Colombia. Primate Conservation. Vol. 6, 42-50.

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Johns, A. 1986. Primates and forest exploitation at Tefe, Brazilian Amazonia. Primate Conservation. Vol. 6, 27-29.

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Kinzey, W.G. 1977. Diet and Feeding Behavior of Callicebus torquatus. in Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys, and Apes. ed T.H. Clutton-Brock. Academic Press: London.

Kinzey, W.G. 1978. Feeding Behavior and Molar Features in Two Species of Titi Monkey. In Recent Advances in Primatology, Vol. 1. eds. D.J. Chivers and J. Herbert. Academic Press.

Kinzey, W.G. 1981. The Titi Monkeys, Genus Callicebus. in Ecology and Behavior of Neotropical Primates Vol. 1. Eds. A.F. Coimbria-Filho and R.A. Mittermeier. Academia Brasileira de Ciencias.

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Kinzey, W.G. 1997. Callicebus. in New World Primates: Ecology, Evolution, and Behavior. ed. Warren G. Kinzey, Aldine de Gruyter, New York.

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Kinzey, W.G. and Wright, P.C. 1982. Grooming behavior in the titi monkey (Callicebus torquatus). American Journal of Primatology. Vol. 3, 267-275.

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Milton, K. and Nessimian, J.L. 1984. Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from northwestern Amazonia. American Journal of Primatology. Vol. 6, 367-371.

Palacios, E., Rodriguez, A., and Defler, T.R. 1997. Diet of a Group of Callicebus torquatus lugens (Humboldt, 1812) During the Annual Resource Bottleneck in Amazonian Colombia. International Journal of Primatology Vol. 18, 503-522.

Soini, P. 1982. Primate conservation in Peruvian Amazonia. International Yearbook of Anthropology. Vol. 22, 37-47.

Starin, E.D. 1978. Food transfer by wild titi monkeys (Callicebus torquatus torquatus). Folia Primatologica. Vol. 30, 15-151.

Last Updated: April 25, 2007.
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