SOCIAL ORGANIZATION AND BEHAVIOR
The titi monkeys are a
monogamous species that presumably mate for life and live
in groups of two to seven individuals consisting of a pair of adults and their
offspring (Wright 1984a; Mason & Mendoza 1993; Kinzey 1997; Bossuyt 2002).
However, groups with several resident adult males are known (Bicca-Marques et
al. 2002). A dominance hierarchy between adults is not observed (Kinzey 1981;
Kinzey 1997). Dispersal from the natal group occurs between two and four years
of age with females dispersing somewhat earlier than males (Wright 1985; Bossuyt
2002). No overt pressure to disperse is exhibited by other group members
Photo: Sean Flannery
Adult monogamous pairs are very close emotionally to one another, coordinating
their activities to a high degree and remaining within close proximity (Mason
1966; Cubicciotti & Mason 1978; Anzenberger et al. 1986; Mendoza et al. 2002).
In addition to coordination of activities, the pair will frequently huddle,
intertwine tails, groom and hold hands. Also, they will foot grasp, lip-smack,
nuzzle, gently grasp one another and sit pressed together in addition to
agonistically responding to strangers (Mason 1966; Mason 1968; Anzenberger et
al. 1986; Fernandez-Duque et al. 1997). An indicator of the strength and
importance of the bond between the mating pair is the significant distress and
agitation they exhibit when they are separated (Mendoza & Mason 1986). In
captivity, when an interloper approaches the mate of a male, the male will show
a marked increase in attraction to its mate and will act agonistically toward
the intruder. Females show the opposite trend, with an increase in attraction
to her counterpart when intruders are farthest away. Females tend to tolerate
intruder females while males display "jealousy" behavior toward non-group adult
males (Cubicciotti & Mason 1978). In addition, males tend to respond to and
react to changes in social conditions faster and to a greater degree than
females and often place themselves between a stranger and the mate (Anzenberger
et al. 1986; Fernandez-Duque et al. 2000).
Titis are cautious in the face of new situations, and approach the unfamiliar
slowly and tentatively. This behavior is probably a result of their small and
exclusive home ranges without
conspecific competitors (Visalberghi & Mason 1983;
Mendoza et al. 2002).
Titis perform a characteristic bout of vocalizations at the outer
boundary of their relatively small range to define and reinforce the boundaries
between their home range and that of other titi groups (Robinson 1977; 1979;
Mason & Mendoza 1993; Lawrence 2007). Shortly after awakening in the morning, titi groups move
to the periphery of their home range and the adults start calling (Robinson
1977). Vocalizations are traded between groups at the boundary for a time as
well as jump displays, long stiff-legged jumps and other, often noisy displays
(Mason 1966; Robinson 1979a). When confronting another group, titis may also
display piloerection, tail-lashing, sustained calling, and chasing (Mason 1966;
Mason & Mendoza 1993). Chasing of individuals from other groups is uncommon and
after the exchange between groups, contact is broken off and groups spend the
rest of their day away from the outer boundary of the home range (Robinson
In captivity, social play occurs only between adult and sub-adult group members
and juveniles, never between the two adults in the group. Grooming occurs
throughout the day, especially during periods of group rest (Kinzey 1981). The
mating pair prefers to groom one another than any other group members and
infants prefer to groom the father (Welker et al. 1998b). Affiliative behaviors
include close proximity, huddling, grooming, and tail twining. Agonistic
behaviors include arching displays, tail lashing, "moaning" and duetting
(Anzenberger et al. 1986). In the wild during the dry season, playing,
intergroup fighting and calling are reduced (Wright 1989). Either sex of the
mating pair can lead the group's movement over the course of the day (Mason
Photo: California NPRC
In captivity, the monogamous titi monkey gives birth around one year after
pairing with a new mate (Valeggia et al. 1999). Females are physically capable
of reproduction as early as two years old; however, if remaining with their
natal group past that age, they cannot reproduce (Welker et al. 1998; Valeggia
et al. 1999). In captivity, the mean age at first birth around 4 years of age
(Welker et al. 1998; Valeggia et al. 1999). Females can reproduce as old as 18
years and males up to 22 years old (Welker et al. 1998). The
in both the wild and in captivity averages around one year (Wright
1985; Valeggia et al. 1999). Mating by a female with a male of another group
has been observed in the wild during the early morning boundary confrontation
but mating of this type is uncommon (Mason 1966; Lawrence 2007). Solicitation of the female by
the male includes manipulating, smelling, or licking the female's genitals and
attempting to mount her (Mason 1966). There is evidence of the possible
presence of seasonality in births in both captivity and the wild which implies a
mating season. In captivity, births can occur year round (Mason 1966; Valeggia
et al. 1999). In the wild a birth peak is observed just prior to the rainy
season, but no discrete breeding season is observed (Wright 1984a). The birth
of twins is uncommon but possible and has been observed in the wild (Knogge &
Heymann 1995). The gestation period of captive titi monkeys has been estimated
at around 128 days (4.2 months) with an average ovarian cycle of female titi
monkeys lasting around 17 days (.56 months) (Jantschke et al. 1995; Valeggia et
al. 1999). Female titis do not menstruate nor do they exhibit sexual swelling
(Valeggia et al. 1999).
Perhaps the most important aspect of titi monkey parenting is the high level of
involvement and importance of the father and his role as predominant carrier and
protector of the infant (Fragaszy et al. 1982; Wright 1984a; Mendoza & Mason
1986a; Mason & Mendoza 1993). In the wild, infants are exclusively carried by
the male except during grooming and nursing by the mother (Mason 1966;
unpublished data cited in Tirado Herrera & Heymann 2004). In captivity, infants
are found the majority of the time in contact with the father and interaction
with the mother is best described as infrequent (Fragaszy et al. 1982).
Starting in the first week of life, the father becomes the predominant carrier
of the infant and the mother only carries the infant for 20% the first week
postpartum. The role of carrier is fully assumed by the father within several
weeks of birth (Mendoza & Mason 1986a). Little care is provided the infant by
siblings and even contact with them in the first three months is limited
(Fragaszy et al. 1982; Mendoza & Mason 1986a). There is some indication that
the curiosity of siblings about the infant is stronger than their desire to
carry the neonate although they have been seen carrying their infant sibling
(Meritt 1980). The more experienced the mother, the less interaction she has
with the infant, and often the only carrying they participate in is related to
suckling. Over half of the time spent by the infant with the mother is spent
suckling (Meritt 1980). To allow the infant access to the nipple, the mother
will raise her arm in a characteristic suckling posture (Fragaszy et al. 1982;
Mason & Mendoza 1993). The father will transport the infant to the mother to
suckle and either parent will jump to the ground to rescue an infant that has
fallen (Jantschke et al. 1995). After the infant is one month old, maternal
contact is mostly limited to brief nursing contact and she is only tolerant of
the infant for short periods of time (Mendoza & Mason 1986b). The strength of
attachment of the infant with its father is indicated by the higher levels of
stress experienced by an infant upon separation from its father than when
separated from its mother (Hoffman et al. 1995). However, it is important to
note that exceptions do exist to the aforementioned pattern of male-focused care
and in some cases the female has been observed caring for the infant as much as
the male (Mason & Mendoza 1993). Interestingly, the parents appear to be more
attached to one another than to their infant (Mendoza & Mason 1986).
Photo: A. M. Stevens
At birth, the captive infant weight averages between .075 kg (.17 lb) and .1 kg
(.22 lb) which is about ten percent of the weight of the mother (Fragaszy et al.
1982; Jantschke et al. 1995). Birth occurs in captivity during the night but
the only observed wild titi birth occurred during the day, during a group
resting period (Meritt 1980; Ruíz et al. 2004). At birth, the neonate is
covered with short, dense and fine hair (Meritt 1980). Newborn infants will
cling ventrally to the neck of the carrier and after the first few weeks will
move to a more dorsal carrying position, usually riding across the shoulders
(Fragaszy et al. 1982; Mason & Mendoza 1993). Transfer from one carrier to
another is characterized by one individual sitting next to the other and the
infant climbing between them (Fragaszy et al. 1982). Captive group contact with
the infant is observed from the day of birth and includes inspection, nuzzling,
and grooming (Fragaszy et al. 1982).
In captivity, infants start spending more than half of their time alone at an
age of about 2 months and independent movement starts at this time (Fragaszy et
al. 1982; Jantschke et al. 1995). By the third or fourth month, running and
leaping are seen (Fragaszy et al. 1982). By around the 29th day of life, the
infant's ears will unfold and by day 37 of life, the infant's pelage is
comparable to that of the adults (Merrit 1980). In the fourth week of life the
infant will first explore independently, but remaining quite close to the father
and not traveling independently (Wright 1984b). Water is first imbibed around
day 69 and solid food is first consumed at day 76 (Merrit 1980). By the 15th
week of life, social play between the infant and juvenile commences and may
include chasing, batting, and gentle biting, and occasionally the father may
also play with the infant. Between 4 and 5 months of age, the infant starts
displaying adult-type interactions with other group members and will start
sitting next to, as opposed to on, them (Fragaszy et al. 1982). Also around
four months old, infants will only be carried by the father during leaping or
when in danger (Wright 1984a). Carrying by other group members persists into
the 6th month of life (Jantschke et al. 1995). Active discouragement of
suckling by the infant by the mother is frequent in the fourth to fifth month of
life and captive weaning
in titis is complete by 12-16 weeks of age (Meritt
1980; Fragaszy et al. 1982). The mother typically will not share food with the
infant while the father will often do so (Wright 1984b). Once dispersed from
the natal group, the juvenile faces potential aggression if it returns (Mayeaux
et al. 2002).
Titi communication has been studied both in captivity and in the wild. Their characteristic
complex vocal behavior has been well documented (e.g. Moynihan 1966; Robinson 1977; 1979b;
Müller 1995; Müller & Anzenberger 2002) and has been said to represent, "the maximum elaboration
and complexity which can be attained by a species specific...language" (Moynihan 1966:125).
Their large repertory of vocalizations can be broadly classified into two types; high-pitched
quiet calls and low-pitched loud calls (Robinson 1977; 1979b). Most loud and quiet vocalizations
are repeated to form phrases and combined into long or short sequences that are used in different
contexts (Robinson 1979b).
Quiet, higher-pitched calls include "squeaks," "whistles," "trills," "chirps," "grunts," "sneezes,"
and distress calls uttered by infants (Robinson 1977). Higher-pitched calls are arranged along a
continuum by type and are not necessarily completely distinct from one another at a discrete point
(Moynihan 1966). Most of these calls are uttered when disturbed, both mildy and significantly.
However, some quiet calls are elicited before and after group calling, while foraging, or when
locating other individuals of the group (Moynihan 1966; Robinson 1977). Specifically, "chirps"
occur while foraging (Robinson 1977; 1979). "Whistles", "squeaks", "sneezes", and "trills" are
presumably uttered in the context of violence or hostility, or in inter- and intra-group conflicts
(Moynihan 1966; Robinson 1977). "Whistles" can also be heard during vigorous social grooming bouts,
vigorous play wrestling, when females resist unwelcome copulation attempts, or when an individual
is lost (Moynihan 1966).
Loud calls include "chirrups", "moans", "pants", "honks", "bellows", "pumps", and "screams", and are
both used in intra- and inter-group long range signaling. "Chirrups", which have been suggested to
contain information on the age and sex of the emitter, are produced in both hostile and non-hostile
situations, such as locating and recognizing group members, and probably fosters group cohesion
(Moynihan 1966; Robinson 1979b). "Moans" can be also heard in a combination of both hostile and
non-hostile circumstances, including during copulation and in greeting or when sympatric primates
pass through the titi's immediate area (Moynihan 1966; Robinson 1979b). Tooth "gnashing" represents
another form of audible communication, and while not vocal, is associated with "moan" vocalizations
and is performed in many of the same circumstances (Moynihan 1966). Screams are uttered in the
context of violence, conflict or hostility, as during fighting between young males (Robinson 1979).
Photo: Gustl Anzenberger
A key feature of the vocal communication of the titi monkey is the ritualized bout of morning
calling and duetting which helps regulate the spacing of groups and their home ranges (Robinson
1981). Duets are long sequences of loud calls that include "chirrups", "grunts", "moans",
"pants", "honks", "bellows", and "pumps." Males start vocalizing "moans" which lead on to male
"bellows" at the boundary of the group's home range and if a neighboring group approaches, both
the female and male will begin duetting in close proximity to one another (Robinson 1977; 1981;
Müller & Anzenberger 2002). Their calls in the duets are not synchronous and both sexes are
capable of producing the same types of vocalizations including both "bellows-and-pumping" and
"pant-and-pumping" (Müller 1995; Müller & Anzenberger 2002). These calls also tend to provoke
quick responses from other groups of titi monkeys and often begin with "moans" and quickly
increase in intensity, lasting up to and longer than five minutes (Moynihan 1966; Mason 1966).
After the confrontational duetting bouts between groups, a characteristic "gobbling" or "pumping"
vocalization may be uttered and is echoed quickly by neighboring groups within earshot (Mason 1966).
Infants vocalize mostly when they are unaccompanied by a parent (Hoffman et al. 1995).
Infants and young juveniles' vocalizations may include "purrs" uttered when being carried by a
non-parent to show discomfort (Moynihan 1966). Distress calls resemble a "buzz" and "chirps"
are vocalized when rejected for carrying by a group member (Robinson 1977; Jantschke et al. 1995).
LISTEN TO VOCALIZATIONS
There are some indications of
olfactory communication in the titi monkey as
evidenced by chest-rubbing and social sniffing (Moynihan 1966; Kinzey 1981).
Titis possess a gland on their sternum that they rub on branches by pressing
their chest to the substrate and propelling themselves forward (Moynihan 1966;
Mason 1966; 1968). Ostensibly, this deposits some substance on the branch to
communicate some olfactory message. The titi also may rub its fist on its chest
and in turn, rub its fist on a branch (Robinson personal communication cited in
Kinzey 1981). While the depositing monkey may smell his deposited scent,
conspecifics have not been seen responding to possible markings left in this
manner (Mason 1968). The other form of potential olfactory communication
involves the sniffing of others, often of the genital region (Moynihan 1966).
Most of the titi visual signals are produced in hostile or agonistic
circumstances (Moynihan 1966). The visual signal repertoire of the titi
includes "swaying," "looking-away," "head-down," "displacement-scratch," "head &
body shake," "eye-closing," "protruding-lips," "baring-the-teeth,"
"arch-posture," "tail-raising," "tail-lashing," and "pilo-erection" (Moynihan
1966; Mason 1968). Mouth-to-mouth contact between adults and infants and
between adults is seen possibly as a greeting or appeasement gesture (Fragaszy
1976; Fragaszy et al. 1982). Another captive behavior that may have a visually
communicative purpose is that of the "general shakes" in which adults will shake
its entire body and head upon the approach of humans (Moynihan 1966).
Content last modified: December 19, 2007
Written by Kurt Gron. Reviewed by Gabriela de Luna.
Cite this page as:
Gron KJ. 2007 December 19. Primate Factsheets: Dusky titi (Callicebus moloch) Behavior . <http://pin.primate.wisc.edu/factsheets/entry/dusky_titi/behav>. Accessed 2014 October 1.