Dusky titi monkey

This sheet covers all species in the Callicebus moloch, Callicebus cupreus and Callicebus donacophilus groups

TAXONOMY

Suborder: Haplorrhini Infraorder: Simiiformes Family: Pitheciidae Subfamily: Callicebinae Genus: Callicebus Species: C. aureipalatii, C. baptista, C. bernhardi, C. brunneus, C. caligatus, C. cinerascens, C. cupreus, C. discolor, C. donacophilus, C. dubius, C. hoffmannsi, C. modestus, C. moloch, C. oenanthe, C. olallae, C. ornatus, C. pallescens, C. stephennashi Other names: titi monkey, luca luca, lucachi; callicèbe (French); springaffe (German); zogue-zogue (Spanish); C. aureipalatii: golden palace monkey, Madidi titi monkey; C. baptista: Baptista lake titi; C. bernhardi: Prince Bernhard’s titi monkey; C. brunneus: brown titi monkey; brun springapa (Swedish); C. caligatus: booted titi, chestnut-bellied titi; brunbröstad springapa (Swedish); C. cinerascens: ashy black titi, ashy titi, ashy-grey titi; askgrå springapa (Swedish); C. cupreus: coppery titi monkey, red titi monkey; callicébe roux (French); roter springaffe, kopferfürbiger springaffe (German); kopparspringapa, röd springapa (Swedish); C. discolor: red titi; socayo, songo songo (Spanish); C. donacophilus: Bolivian grey titi, Bolivian titi monkey, white-eared titi; vitörad springapa (Swedish); C. dubius: doubtful titi monkey, dubious titi, Hershkovitz’s titi; vitpannad springapa (Swedish); C. hoffmannsi: Hoffmann’s titi monkey; gulbröstad springapa, Hoffmanns springapa (Swedish); C. modestus: Bolivian titi, modest titi, Rio Beni titi, mono tití (Spanish); Boliviansk springapa, gråbrun springapa (Swedish); C. moloch: dusky titi, red-bellied titi; grijze springaap (Dutch); titi molock (French); grå springapa, mörk springapa, orabassn (Swedish); C. oenanthe: Andean titi monkey, Rio Mayo titi; sugkamat (Aguaruna); bergsspringapa (Swedish); C. olallae: Beni titi monkey, Olalla’s titi, Ollala brothers’ titi; mono tití (Spanish); benispringapa, Olallas springapa (Swedish); C. ornatus: ornate titi monkey; C. pallescens: white-coated titi; C. stephennashi: Stephen Nash’s titi monkey.

---

---

This sheet covers all species in the Callicebus moloch, Callicebus cupreus and Callicebus donacophilus groups

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 (Bossuyt 2002). 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 1979a). 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 1966). REPRODUCTION 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 interbirth interval 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).

PARENTAL CARE

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). 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).

COMMUNICATION

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). 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

• Callicebus discolor duet  (Di Fiore & Fernandez-Duque)

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 2020 July 30.

This sheet covers all species in the Callicebus moloch, Callicebus cupreus and Callicebus donacophilus groups.

INTERNATIONAL STATUS

For individual primate species conservation status, please search the IUCN Red List. Also search the current scientific literature for primate conservation status (overall as well as for individual species), and visit CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora).

Conservation information last updated in 2007 follows, for comparison:

CONSERVATION THREATS

Threat: Human-Induced Habitat Loss and Degradation

As with other neotropical primates, deforestation and loss of habitat are profound threats to the survival of the titi monkey. In Brazil, the government’s plan to pave, improve, and construct over 6000 km of roads will likely exacerbate deforestation by facilitating logging and forest fires, and moving many more people and potentially destructive activities into formerly remote areas (Nepstad et al. 2001). This pattern follows elsewhere in the titi range, where highway building or improvement in Bolivia, Peru and Brazil alike have also caused or have the potential to cause increased destruction of habitat (van Roosmalen et al. 2002; Mark 2003; Felton et al. 2006; Wallace et al. 2006). In Paraguay, deforestation is again the largest threat to endemic primates (Stallings 1985). Deforestation due to agriculture poses a significant threat to titis, especially rice growing, which is typically undertaken near rivers and streams; habitats used by titis (Mark 2003). In Colombia, illegal coca farms are quite widespread and numerous, often located within titi habitats. While some efforts have been targeted at eliminating such illegal farms, these have lead to hostility with farmers, confounding conservation. Spraying to kill coca has also harmed the natural habitats near the farms (Defler et al. 2003). Coffee plantations utilize slash-and-burn clearing techniques and can completely destroy the forest habitats of titis. In addition, wood is the preferred building and fuel source, so even where fragmented forests remain, they are under threat of destruction to those ends (DeLuycker 2006). Governmental farming expansion programs and road expansion also threaten titis by encouraging human immigration to areas near titi habitats and result in a transition from traditional land use to more intensive agriculture and different settlement patterns which increase deforestation (Rengifo Ruiz 1994 cited in DeLuycker 2006; Rowe & Martinez 2003; DeLuycker 2006). Sometimes, titi habitats are fragmented and surrounded by grazing lands. The results of this are mixed in relation to conservation however, as ranchers sometimes prevent hunting on their lands and it appears that titis are adaptable and are able to travel on the ground between forest fragments (Felton et al. 2006). In addition, some evidence points to the ability of some titis to thrive in disturbed habitats near human activities (van Roosmalen et al. 2002). This is not to say that fragmentation is not dangerous however, as fragmentation can prevent the establishment of new territories and reproductive opportunities by titis (DeLuycker 2006). Petroleum prospecting and extraction in addition to other infrastructure development also threaten titi populations in formerly untouched areas as do potential hydroelectric projects (Defler et al. 2003; Rowe & Martinez 2003; Marsh 2004; Felton et al. 2006; Wallace et al. 2006). It has been suggested that the creation of forest corridors connecting isolated forest remnants would be an effective means by which to help ensure the survival of titis (DeLuycker 2006). Conservation should also focus on the protection of populations in such fragments (Mark 2003). In addition, governmental reward systems designed to promote forest conservation and the establishment of such corridors would be a step in the right direction for titi conservation (DeLuycker 2006). It is estimated that to sustain a viable population of titis, a contiguous area of at a minimum 81 km² (31.3 mi²) is required (Stallings 1985). In some cases it is hard to enforce protective legislation however, due to civil unrest, drug activity, and insurgents, as is the case in some areas of Colombia (Defler et al. 2003).

Threat: Harvesting (hunting/gathering)

Hunting is also a threat to titis, mostly for subsistence (Rowe & Martinez 2003). Often the take by indigenous populations is quite low and not a serious threat, as in Paraguay (Stallings 1985). However, the threat from over-hunting remains and hunting pressure on titis in some areas is quite intense (Rowe & Martinez 2003). Indeed, some populations have become extinct as a result of unchecked hunting (Felton et al. 2006). Due to their small size, titis are also kept and commercially sold as pets, representing a potentially serious threat to their numbers (Kohlhaas 1988; Stallings 1985; Rowe & Martinez 2003). One captive family of titis captured in Peru was offered for sale at a price of less than $10 (Rowe & Martinez 2003).

LINKS TO MORE ABOUT CONSERVATION

CONSERVATION INFORMATION

• No current links for Callicebus moloch
• Links for all species

CONSERVATION NEWS

• Photos: researchers uncover top priority areas for Bolivian primates  (Mongabay; June 28, 2010)
• Links for all species

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) Conservation . <http://pin.primate.wisc.edu/factsheets/entry/dusky_titi/cons>. Accessed 2020 July 30.

This sheet covers all species in the Callicebus moloch, Callicebus cupreus and Callicebus donacophilus groups

This sheet covers all species in the Callicebus moloch, Callicebus cupreus and Callicebus donacophilus groups