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Callicebus donacophilusBolivian titi

By Nicholas Venturelli

Geographic Range

Bolivian titi monkeys, Callicebus donacophilus, are primarily found in eastern Bolivia in the upper basins of the Mamore River and the Rio Grande. They may also be found in the extreme southwestern parts of the Brazilian states of Mato Grasso and Rondônia. (Ferrari, et al., 2000; Hershkovitz, 1990)

Habitat

Bolivian titi monkeys inhabit riparian zones and gallery forests near swampy grasslands and other open areas. (Ferrari, et al., 2000)

Physical Description

Bolivian titis are small, New World monkeys , averaging about 320 mm in length. Males are only slightly larger than females, weighing on average 991 g while females weigh 909 g. Titis have long tails that are not prehensile. They have very little prognathism and long skulls. Titi monkeys have long hind limbs with an intermembral index of 75.

The chest and belly of Bolivian titi monkeys is completely orange to brown-orange while the dorsal side and extremities range from grey to orange agouti in color. The tail may include black or grey coloring, and they have white tufts on their ears.

The dental formula of Bolivian titis, as with other titi monkeys, is 2.1.3.3/2.1.3.3. Compared to other platyrrhines, the canines of titi monkeys are relatively short and their molars are fairly simple.

Bolivian titi monkeys can be distinguished from closly related speices including Callicebus olallae, Callicebus brunneus, and Callicebus modestus by their well-developed malar stripe and lack of distinct sideburns. (Fleagle, 1999; Hershkovitz, 1990; van Roosmalen, et al., 2002)

  • Sexual Dimorphism
  • sexes alike
  • Average mass
    Males 991 g; Females 909 g
    oz
  • Average length
    320 mm
    12.60 in

Reproduction

Like all titi monkeys, Bolivian titis are monogamous. A strong bond is formed between male and female partners, which generally mate for life. They remain in close proximity to one another for almost all of their activities and often rest together with hands clasped and tails interwoven in a characteristic manner known as “twining.” They also have been observed grasping feet, nuzzling, and lip-smacking. When apart, they display physical signs of anxiety and distress. Titi monkeys also exhibit “jealous” behavior when approached by a stranger, especially the male, who mounts and tightly grasps his mate in the presence of another individual to prevent “extramarital” relations. (Anzenberger, et al., 1986; Mendoza, et al., 2002; Valeggia, et al., 1999)

In captivity, Bolivian titi monkeys breed throughout the year. In the wild, a breeding season is predicted, perhaps in the spring preceding the rainy season in Bolivia. In captivity, female titi monkeys give birth approximately one year after finding a mate. After a gestation period of about 18 weeks, females give birth to a single offspring, though twins are uncommon. Although female Bolivian titi monkeys reach sexual maturity at 2 years of age, the mean age of first birth is 4 years. (Gron, 2007; Valeggia, et al., 1999)

  • Key Reproductive Features
  • gonochoric/gonochoristic/dioecious (sexes separate)
  • sexual
  • viviparous
  • Average number of offspring
    1
  • Average gestation period
    18 weeks
  • Range age at sexual or reproductive maturity (female)
    2 (low) years
  • Average age at sexual or reproductive maturity (female)
    4 years

Male Bolivian titi monkeys play a dominant role in the care of their young. Although females nurse their offspring, males are the principal carriers and protectors of their young. During the first week of life, mother Bolivian titi monkeys carry their infants only 20% of the time, and after the first month, maternal contact is scarce. Infants experience more stress and elevated heart rates when separated from their father than from their mother, with few exceptions. Bollivian titi monkeys experience a stronger bond with their mate than with their offspring. (Mendoza and Mason, 1986)

Lifespan/Longevity

The oldest Bolivian titi in captivity reached 24.8 years of age. Little information is available regarding the lifespan of this species in the wild. Other members of the genus Callicebus, such as Callicebus moloch, live an average of 25 years. (Gron, 2007; de Magalhaes, et al., 2009)

  • Average lifespan
    Status: captivity
    25 years

Behavior

Bolivian titi monkeys may live in family groups of 2 to 7 members. Although males exhibit some degree of leadership in these groups, no dominance hierarchy has been observed between sexes or among individuals. Adult titi pairs remain close to each other throughout life and coordinate their activities so as to not spend a great amount of time physically apart. Members of a mated pair often entwine their tails during sleep. Bolivian titis generally sleep close to their group members in the vines of small branches.

Like most New World Monkeys, Bolivian titis are diurnal, with daily activity lasting an average of 11.5 hours. Titis wake early in the morning around sunrise and remain active until sunset. They generally divide the day into two main feeding times with a rest during midday.

Bolivian titi monkeys are arboreal and quadrupedal, primarily traveling through the lower levels of the forest. They are rarely seen on the ground. Locomotion generally consists of short leaps, for which their long hind limbs are well-adapted, and they also walk and climb. Because their tails are not prehensile, the tail does not come into contact with the surface on which they are walking.

Titi monkeys have small home ranges, and they do not exhibit considerable curiosity. They are wary and hesitant to approach new situations. They are, however, territorial and utilize a variety of vocalizations to define and reinforce their territory. (Anzenberger, et al., 1986; Kinzey, 1978; Kinzey, 1981; Valeggia, et al., 1999; Youlatos, 1999)

  • Range territory size
    0.005 to 0.14 km^2

Home Range

The home range of Bolivian titis averages 0.005 to 0.14 km^2, while their day range averages between 0.5 and 1.5 km. (Gron, 2007; Kinzey, 1978)

Communication and Perception

Titi monkeys, including Bolivian titis, utilize a variety of vocalizations in order to communicate. These vocalizations are complex and numerous, though they are generally classified into two groups: the higher pitched squeaks, trills, chirps, and grunts; and the lower pitched chirrups, moans, pants, honks, bellows, pumps, and screams. Higher pitched sounds tend to be employed when they are agitated or encounter violence. Lower pitched, louder sounds are often used in intra-group signaling as well as contacting other social groups over a long range. Certain chirrup sounds are believed to reveal information about the age and sex of the calling monkey and can be used to locate group members. Moans can be heard during copulation and greeting.

Titis perform a characteristic bout of vocalizations at the outer boundary of their relatively small range to define and reinforce the boundaries of their home range. This generally occurs in the morning soon after awakening. A male emits loud calls, moans, grunts, and other vocalizations in order to establish the boundaries. If a neighboring group draws near, the groups participate in what is known as "duetting", with both groups calling. As the groups draw together, the intensity of this duetting increases and both males and females participate. If two groups directly confront each other, more physical communication is exhibited included tail-lashing, piloerection, chasing, and further calling.

Titi monkeys also use physical communication, including grooming and tail entwining. Male and female mates show a strong preference for grooming and entwining with each other rather than with other members of their group. (Moynihan, 1966; Müller and Anzenberger, 2002; Robinson, 1979)

  • Other Communication Modes
  • duets

Food Habits

Bolivian titi monkeys are primarily frugivorous, and it is estimated that their diet consists of over 70% fruit. They also eat leaves, seeds, and insects. Much of the day is spent resting in order to digest their mostly herbivorous diet. (Wright, 1989)

  • Animal Foods
  • insects
  • Plant Foods
  • leaves
  • seeds, grains, and nuts
  • fruit

Predation

Many species of raptors prey on titi monkeys, like Bolivian titi monkeys, including Guianan crested eagles and ornate hawk eagles. Other predators include felids such as jaguars as well as various arboreal snakes. Predation on infants by tufted capuchins has also been observed. Bolivian titis are have a cryptic coloration, helping them to blend in with their surroundings and avoid predation. (Gron, 2007)

  • Anti-predator Adaptations
  • cryptic

Ecosystem Roles

Titi monkeys, including Bolivian titis, can coexist with many other New World monkeys including marmosets, tamarins, squirrel monkeys, capuchins, owl monkeys, howler monkeys, woolly monkeys, and spider monkeys. However, some of these larger species often chase titi monkeys away from fruit trees and other sources of food. Because titi monkeys prefer to remain isolated within their social group, they attempt to avoid contact with other primates.

Because they are frugivores, Bolivian titi monkeys may play a small role in seed dispersal.

The main parasites found in neotropical primates, including Bolivian titi monkeys, are trypanosomes (Trypanosoma cruzi, Trypanosoma rangeli, Trypanosoma minasense, and Trypanosoma devei), which are a prevalent cause of infection. (Gron, 2007; Wright, 1989; Ziccardi, et al., 2000)

  • Ecosystem Impact
  • disperses seeds
Commensal/Parasitic Species
  • Trypanosoma cruzi
  • Trypanosoma rangeli
  • Trypanosoma minasense
  • Trypanosoma devei

Economic Importance for Humans: Positive

Bolivian titi monkeys may play a part in drawing tourists to forested areas of Bolivia.

Economic Importance for Humans: Negative

There are no known adverse effects of Bolivian titi monkeys on humans.

Conservation Status

Although populations are declining, Bolivian titi monkeys are listed by the IUCN as a species of least concern. They have a relatively wide range and a slowly declining population. Bolivian titi monkeys have proven fairly adaptable, and they have a low number of natural predators. Their main threat is attributed to habitat loss due to agriculture. Bolivian titi monkeys are one of three primate species that survive within and around the borders of cities and rural human establishments in this region. (Veiga, et al., 2008)

Contributors

Nicholas Venturelli (author), Yale University, Eric Sargis (editor), Yale University, Gail McCormick (editor), Animal Diversity Web Staff.

Glossary

Neotropical

living in the southern part of the New World. In other words, Central and South America.

World Map

acoustic

uses sound to communicate

arboreal

Referring to an animal that lives in trees; tree-climbing.

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

chemical

uses smells or other chemicals to communicate

cryptic

having markings, coloration, shapes, or other features that cause an animal to be camouflaged in its natural environment; being difficult to see or otherwise detect.

diurnal
  1. active during the day, 2. lasting for one day.
duets

to jointly display, usually with sounds in a highly coordinated fashion, at the same time as one other individual of the same species, often a mate

endothermic

animals that use metabolically generated heat to regulate body temperature independently of ambient temperature. Endothermy is a synapomorphy of the Mammalia, although it may have arisen in a (now extinct) synapsid ancestor; the fossil record does not distinguish these possibilities. Convergent in birds.

female parental care

parental care is carried out by females

forest

forest biomes are dominated by trees, otherwise forest biomes can vary widely in amount of precipitation and seasonality.

frugivore

an animal that mainly eats fruit

herbivore

An animal that eats mainly plants or parts of plants.

male parental care

parental care is carried out by males

monogamous

Having one mate at a time.

motile

having the capacity to move from one place to another.

native range

the area in which the animal is naturally found, the region in which it is endemic.

omnivore

an animal that mainly eats all kinds of things, including plants and animals

rainforest

rainforests, both temperate and tropical, are dominated by trees often forming a closed canopy with little light reaching the ground. Epiphytes and climbing plants are also abundant. Precipitation is typically not limiting, but may be somewhat seasonal.

riparian

Referring to something living or located adjacent to a waterbody (usually, but not always, a river or stream).

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

social

associates with others of its species; forms social groups.

tactile

uses touch to communicate

tropical

the region of the earth that surrounds the equator, from 23.5 degrees north to 23.5 degrees south.

visual

uses sight to communicate

viviparous

reproduction in which fertilization and development take place within the female body and the developing embryo derives nourishment from the female.

References

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

Ferrari, S., S. Iwanga, M. Messias, E. Ramos, P. Ramos, E. da Cruz Neto, P. Coutinho. 2000. Titi monkeys (Callicebus spp., Atelidae: Platyrrhini) in the Brazilian state of Rondônia. Primates, 41(2): 229-234.

Fleagle, J. 1999. Primate Adaptation and Evolution. San Diego: Academic Press.

Gron, K. 2007. "Primate Factsheets: Dusky titi (Callicebus moloch) Taxonomy, Morphology, & Ecology" (On-line). Accessed April 18, 2011 at http://pin.primate.wisc.edu/factsheets/entry/dusky_titi/taxon.

Hershkovitz, P. 1990. Titis, new world monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zoology, 55: 1-109.

Kinzey, W. 1978. Feeding behaviour and molar features in two species of titi monkey. Pp. 373-85 in D Chivers, J Herbert, eds. Recent Advances in Primatology, Vol. 1. London: Academic Press.

Kinzey, W. 1981. The titi monkeys, genus Callicebus: I. description of the species. Pp. 241-76 in A Coimbra-Filho, R Mittermeier, eds. Ecology and behavior of neotropical primates, Vol. 1. Rio de Janeiro: Academia Brasileira de Ciências.

Mendoza, S., W. Mason. 1986. Contrasting responses to intruders and to involuntary separation by monogamous and polygynous new world monkeys. Physiology and Behavior, 38: 795-801.

Mendoza, S., D. Reeder, W. Mason. 2002. Nature of Proximate Mechanisms Underlying Primate Social Systems: Simplicity and Redundancy. Evolutionary Anthropology, 11: 112-116.

Moynihan, M. 1966. Communication in the titi monkey, Callicebus. Journal of Zoology, 150: 77-127.

Müller, A., G. Anzenberger. 2002. Duetting in the Titi Monkey Callicebus cupreus: Structure, Pair Specificity and Development of Duets. Folia Primatologica, 73: 1-12.

Robinson, J. 1979. Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behavioral Ecology and Sociobiology, 5: 1-15.

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

Veiga, L., R. Wallace, S. Ferrari. 2008. "Callicebus donacophilus" (On-line). In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.4. Accessed April 25, 2011 at http://www.iucnredlist.org/apps/redlist/details/41548/0.

Wright, P. 1989. The nocturnal primate niche in the new world. Journal of Human Evolution, 18(7): 635-58.

Youlatos, D. 1999. Comparative locomotion of six sympatric primates in Ecuador. Annales des Sciences Naturelles, 20(4): 161-8.

Ziccardi, M., R. Lourenço-de-Oliveira, R. Lainson, M. do Carmo de Oliveira Brígido, J. Augusto Pereira Carneiro Muniz. 2000. Trypanosomes of Non-human Primates from the National Centre of Primates, Ananindeua, State of Pará, Brazil. Memórias do Instituto Oswaldo Cruz, 95(2): 157-159. Accessed May 03, 2011 at http://memorias.ioc.fiocruz.br/952/3890.html.

de Magalhaes, J., A. Budovsky, G. Lehmann, J. Costa, Y. Li, V. Fraifeld, G. Church. 2009. The Human Ageing Genomic Resources: online databases and tools for biogerontologists.. Aging Cell, 8(1): 65-72. Accessed May 03, 2011 at http://genomics.senescence.info/species/entry.php?species=Callicebus_donacophilus.

van Roosmalen, M., T. van Roosmalen, R. Mittermeier. 2002. A taxonomic review of the titi monkeys, genus Callicebus Thomas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neotropical Primates, 10: (suppl.).

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