(Atelidae)
Class: Mammalia
Order: Primates
Suborder: Anthropoidea
Family: Atelidae
Thumbnail description
The largest New World monkeys, possess prehensile tails; range in color from pale blonde and light gray to black; some have completely black faces, others have pink and white facial mottling
Size
Ateles: head and body length 15–25 in (38–64 cm), tail length 20–35 in (51–89 cm), 13.2 lb (6 kg). Brachyteles: head and body length: 18–25 in (46–64 cm), tail length 23–36 in (59–92 cm), 15.4–33 lb (7–15 kg); Alouatta: head and body length 22–36 in (56–92 cm), tail length 20–35 in (51–89 cm), 8.8–22 lb (4–10 kg). Lagothrix: head and body length: 20–35 in (51–69 cm), tail length 23–28 in (59–72 cm), 12–24 lb (5.5–10.8 kg)
Number of genera, species
5 genera; 22–24 species
Habitat
Gallery forest, deciduous and semi-deciduous rainforest, some species also found in mangrove swamps or secondary forest
Conservation status
Critically Endangered: 3 species; Endangered: 3 species; Vulnerable: 5
Distribution
Mexico through Central and South America
Evolution and systematics
Mid-Miocene deposits of Colombia have yielded material assigned to the fossil genus Stirtonia, but there is little else in the way of fossil Atelidae until more recent Pleistocene fossils from caves in eastern Brazil. One of these, Caipora bambuiorum is considered to be a large juvenile with a distinctly Ateles-like crania. Another, Paratopithecus brasiliensis, is an even larger (approximately 55 lb, or 25 kg) adult, whose post-crania resembles extant Ateles and Brachyteles and some skeletal fragments found in the 1800s in the state of Minas Gerais. The crania of Paratopithecus resembles extant Alouatta, however, leading to uncertainties in interpreting such a mosaic of traits.
The Atelidae is now widely accepted as a monophyletic family, although some prior classifications included variously Pithecinae, Callicebinae, and Aotinae along with the Alouattinae and Atelinae. Alouatta has typically been distinguished from the other genera, but there is still controversy over the phylogenetic relationships among the atelins. Morphological analyses group Ateles and Brachyteles in a clade separate from Lagothrix, while molecular data suggests a Brachyteles/Lagothrix clade. Indeed, the karyotypes of these two genera are similar (2n=62 chromosomes), and differ from Ateles, which varies from 2n=32 to 2n=34 chromosomes.
Like many other primates, the Atelidae has recently undergone a major taxonomic revision. The result, for the most part, has been the splitting of previously recognized subspecies into distinct species, and in the case of Lagothrix, splitting the yellow-tailed woolly monkey, L. flavicauda, into a separate genus, Oreonax flavicauda. In many cases, the reclassifications have been prompted by new molecular analyses, but re-examinations of museum specimens have also played a role.
Physical characteristics
The Atelidae are the largest New World primates. In Alouatta and Lagothrix, females are much smaller than males, while in Ateles and Brachyteles, males and females are more similar to one another in body size. All of the Atelidae possess prehensile tails, which are bare on the distal underside. The tails are very sensitive, and are used for grasping much like an extra hand. All of the atelids also have 36 teeth, with a dental formula of (I2/2 C1/1 P3/3 M3/3). The relative size and shapes of their teeth, as well as their jaws and chewing muscles, vary with their respective feeding adaptations.
Atelidae range in color from pale buff or gray (Brachyteles) to dark black (some Alouatta and Ateles). Some species of Alouatta are sexually dichromatic in body color. Alouatta, Lagothrix, and Brachyteles arachnoides have completely black faces. Oreonax has a lighter muzzle, many species of Ateles have distinctly paler eye patches, and Brachyteles hypoxanthus has pink and white patches of skin in variable patterns on the face. The latter also exhibit variation in pigment on the scrotum.
In both Ateles and Brachyteles females, the clitoris is pendulous and elongated. Male Brachyteles also have relatively large testes. Both of these genera also have long hooked fingers, and long limbs and tails relative to their bodies. Lagothrix and Alouatta have more compact bodies and limbs, and relatively shorter tails. Lagothrix travels by suspensory locomotion much less than Ateles or Brachyteles, but is faster and more agile than Alouatta. Alouatta possesses an enlarged hyoid bone, which contributes to the projection of long distance roars. Alouatta also has an elongated hindgut associated with the slow rate of food passage.
Distribution
The family is found only in Central and South America. Howler monkeys (genus Alouatta) have the most extensive distribution, which ranges from southern Mexico in the north to northern Argentina in the south. Spider monkeys (genus Ateles) occur from southern Mexico, through Central America and the Amazon. Woolly monkeys (genus Lagothrix) are restricted to the Amazon, with the recently recognized genus Oreonax, or the yellow-tailed woolly monkey, found only in the northeastern montane cloud forest of Peru. Muriquis (genus Brachyteles) are found only in the southeastern Atlantic forest of Brazil.
Howler monkeys occur sympatrically with one, and sometimes two of the other genera. Alouatta is the only genus in this family that occurs sympatrically with Brachyteles. In some regions in the Amazon, Alouatta, Ateles, and Lagothrix are found together.
Habitat
All species are arboreal, although Alouatta, Ateles, Brachyteles, and Lagothrix have been observed to descend to the ground to eat, drink, play, and travel for brief periods. With the exception of Oreonax, they are found in a wide variety of habitats. Alouatta and Brachyteles in particular are still found in disturbed and secondary patches of forest, where their ability to consume large quantities of leaves may contribute to their persistence. Lagothrix and Ateles are more restricted to primary tropical rainforest, although some species of Ateles are also found in semi-deciduous and degraded forest patches.
Atelids appear to prefer the upper canopy, but they also use their tails to exploit foods at lower levels in the forest. They tend to rest on secure branches, but are adept at feeding from terminal branches and lianas.
Behavior
All species live in multimale, multifemale groups, although one-male, multifemale groups of Alouatta are also common. In the three well-known atelin genera (Ateles, Brachyteles, and Lagothrix), males are philopatric, while females disperse from their natal groups to join other groups of males. In Alouatta, both males and females disperse from their natal groups, usually to establish new troops. Female red howler monkeys (Alouatta seniculus) may be retained in their natal troops, while males sometimes disperse in pairs to establish new troops together.
Alouatta are renowned for their loud, long-distance roars. Neighboring troops engage in howling displays, often, but not exclusively, at the boundaries of their ranges. Howler monkey calls can be heard by humans as far as 0.6 mi (2 km) away. Ateles and Brachyteles have large repertoires of vocalizations, including a long-distance call that resembles a horse's whinny, and an alarm call that resembles a dog's bark. They also have softer, less far ranging "chuckles," which may help them to maintain contact with one another while they are spread out during travel and foraging.
None of the species defend exclusive territories, although encounters between groups, especially of Alouatta, can be highly aggressive. In Lagothrix, Ateles, and Brachyteles, large neighboring groups exploit large, overlapping home ranges. Home range overlap is greater at high population densities. Home range sizes vary from 25 acres (10 ha) in Alouatta to over 2,220 acres (900 ha) in woolly monkeys and muriquis living in continuous forest in the Amazon and southern Atlantic forest, respectively.
All of the genera are primarily diurnal. Observers that leave the monkeys asleep at dusk often find them in the exact same positions the next morning. Activity patterns differ with climate and season. In general, bouts of morning traveling and feeding are followed by mid-day siestas, and then more traveling and feeding before the groups settle down for the night. Howler monkeys devote up to 70% of their daylight hours to resting, and travel shorter distances each day than the other genera. Spider monkeys and muriquis devote about half of the day to resting, and can travel up to 1.9 mi (3 km) in a day. Woolly monkeys are intermediate in their resting and traveling habitats, at least at the sites where they have been studied to date.
Feeding ecology and diet
All species show clear preferences for ripe fruit when it is available, and supplement their diets with various quantities of leaves. Woolly monkeys at La Macarena, Colombia also consume substantial quantities of insects. Other foods, such as flowers and nectar, and new shoots are eaten when available, while bark and bamboo supplement diets during periods of preferred food scarcity.
Howler monkeys are by far the most folivorous, but the proportion of leaves in their diets varies greatly by habitat. Sympatric species exhibit considerable overlap in diet, feeding on many of the same fruit, leaf, and flower species, sometimes from the same trees or lianas. There are interesting parallels in the proportion of fruits versus leaves in the annual diets of sympatric spider monkeys and howler monkeys, on the one hand, and those of sympatric muriquis and howler monkeys, on the other hand. In each pair, the howler monkeys are substantially more folivorous than either spider monkeys or muriquis.
There is also extensive intraspecific variation in diets. For example, populations of southern muriquis inhabiting disturbed or regenerating forest fragments devote up to 70% of their feeding time to leaves, whereas those inhabiting undisturbed, continuous forest devote up to 70% of their feeding time to fruits. The latter also utilize much larger home ranges, and occur at much lower population densities. Whether low population density permits them to maintain a more frugivorous diet by expanding their home range, or whether undisturbed forests have more abundant fruit is not yet known.
All genera possess prehensile tails, which permit them to feed for long periods of time in suspended postures. Secured by their tails, they can access foods close to the ground or from plants and branches that are too small or flimsy to support their body weights. Their tails also free up their hands, which they can use to sort foods and bring them to their mouths. The atelins also travel by suspensory locomotion, using their arms and tails to swing through the canopy. Suspensory locomotion permits them to travel long distances rapidly, and may contribute to their ability to monitor dispersed patches of preferred fruits. Howler monkeys are quadrupedal, traveling much shorter distances more slowly than the atelins.
Reproductive biology
Females exhibit proceptive behaviors, which in Brachyteles and Ateles are now known to correspond with their ovarian cycles. Males frequently inspect the genitalia of females by visual and olfactory means. Copulations sometimes occur with the females sitting, instead of standing as occurs in most other primates.
Female atelins typically mate with multiple partners, although the degree to which single males monopolize access to females and exclude other males from mating varies greatly. In multimale troops of red howler monkeys, the alpha male can account for 100% of all fertilizations, resulting in the genetic equivalent of a single-male troop. In woolly monkeys and spider monkeys, high-ranking males account for most observed copulations. In muriquis, females mate with multiple partners, often one right after the other, and there is no evidence that males compete overtly with one another for access to mates.
There is no evidence of paternal or allo-parental care among the atelins. However, male howler monkeys will sometimes carry infants or position themselves between infants and extra-troop males, which may threaten infants in their efforts to take over female troops.
Reproductive seasonality varies widely across species and populations of the same species, with a tendency for more seasonal reproduction in more seasonal habitats. It is unclear whether reproductive seasonality reflects maternal condition at the time of conceptions, or the availability of food at the time of weaning. The tendency is for births to occur in the dry season when preferred fruits and new leaves are scarcest, and both conceptions and weaning to occur in the rainy season when preferred foods are most abundant.
Gestation length ranges from 6 months in Alouatta, to 7 months in Ateles, to 7.2 months in Brachyteles. Average inter-birth intervals range from 2 years in Alouatta to 3 years in the atelins. Age at first reproduction for females ranges from about 4 years in Alouatta to at least 9 years in Brachyteles.
Conservation status
Both species of Brachyteles, along with the recently recognized genus, Oreonax, are classified as Critically Endangered based on their highly restricted distributions, small population size, and deteriorating habitats. Brachyteles is the only genus of Atelidae endemic to the Brazilian Atlantic forest. The brown howler monkey, Alouatta guariba, is also endemic to the Atlantic forest, and is classified as Vulnerable. The status of Brachyteles hypoxanthus is probably more critical than that of B. arachnoides because the latter still retains relatively large populations in protected forest. Population estimates for Brachyteles hypoxanthus are under 500 individuals, with nearly 200 found in one small reserve in Minas Gerais. Oreonax population size is estimated at fewer than 300 individuals.
Three species are classified as Endangered (Alouatta coibensis, Ateles marginatus, and A. hybridus) and five species are classified as Vulnerable (Alouatta guariba, Ateles belzebuth, Lagothrix cana, L. lugens, and L. poeppigii). Local populations of several subspecies are also considered to be Endangered or Vulnerable. In all cases, restricted geographic distributions coupled with habitat destruction and hunting pressures contribute to the precariousness of their futures.
The large body size and large group size of atelid make them attractive prey to hunters. In addition to the toll that hunting takes on local populations, many have suffered due to habitat destruction and fragmentation. The construction of roads increases access for hunters and degrades habitats, while the cutting and burning of forest for pasture and agriculture.
Conservation efforts are widespread, and include the establishment of protected parks and reserves as well as legislation that prohibits hunting. However, enforcement of prohibitions is often impeded by insufficient funds. Conservation education efforts and international collaborations between habitat countries and nongovernmental organizations (NGOs) can be effective, but require long-term commitments at all levels.
Significance to humans
Atelidae are represented in the art and legends of the people they live nearby. Their large body size and social habits have probably always made them a source of prized meat. The large testes of Brachyteles were associated with sexual potency, and made into purses by hunters.
None of the Atelidae are considered to be agricultural pests or dangerous to humans. The docile behavior of Ateles and Brachyteles also contribute to their desirability as pets.
Species accounts
Mantled howler monkeyVenezuelan red howler monkey
Geoffroy's spider monkey
Peruvian spider monkey
Southern muriqui
Northern muriqui
Gray woolly monkey
Colombian woolly monkey
Resources
Books:Crockett, C. M. Adaptive Radiations of Neotropical Primates. Edited by M. A. Norconk, A. L. Rosenberger, and P. A. Garber. New York: Plenum Press, 1996.
Crockett, C. M., and T. R. Pope. Juvenile Primates: Life History, Development, and Behavior, edited by M. E. Pereira and L. A. Fairbanks. New York: Oxford University Press, 1993.
Groves, C. Primate Taxonomy. Washington, DC: Smithsonian Institute Press, 2001.
Hartwig, W. C., A. L. Rosenberger, P. A. Garber, and M. A. Norconk. Adaptive Radiations of Neotropical Primates, edited by M. A. Norconk, A. L. Rosenberger, and P. A. Garber. New York: Plenum Press, 1996.
Nowak, R. M. Walker's Primates of the World. Baltimore: The Johns Hopkins University Press, 1999.
Peres, C. A. Adaptive Radiations of Neotropical Primates. Edited by M. A. Norconk, A. L. Rosenberger, and P. A. Garber. New York: Plenum Press, 1996.
Rowe, N. A Pictorial Guide to the Primates. New York: Pogomias Press, 1996.
Schneider, H., and A. L. Rosenberger. Adaptive Radiations of Neotropical Primates, edited by M. A. Norconk, A. L. Rosenberger, and P. A. Garber. New York: Plenum Press, 1996.
Strier, K. B. Faces in the Forest: The Endangered Muriqui Monkeys of Brazil. Cambridge, MA: Harvard University Press, 1999.
Sussman, R. W. Primate Ecology and Social Structure, Volume 2: New World Monkeys. Needham Heights, MA: Pearson Custom Publishing, 1999.
Periodicals:Campbell, C. J. "Fur Rubbing Behavior in Free-ranging Black-handed Spider Monkeys (Ateles geoffroyi) in Panama." American Journal of Primatology 51 (2000): 205-208.
Campbell, C. J., S. E. Shideler, H. E. Todd, and B. L. Lashley. "Fecal Analysis of Ovarian Cycling in Female Black-handed Spider Monkeys (Ateles geoffroyi)." American Journal of Primatology 54 (2001): 79-89.
Cartelle, C., and W. C. Hartwig. "A New Extinct Primate Among the Pleistocene Megafauna of Bahia, Brazil." Proceedings of the National Academy of Sciences 93 (1996): 6405-6409. ——. "Ecological Constraints on Group Size in Three Species of Neotropical Primates." Folia Primatologica 55 (1990): 1-9.
Chapman, C. A. "Patch Use and Patch Depletion by the Spider and Howling Monkeys of Santa Rosa National Park, Costa Rica." Behaviour 105 (1988): 99-116.
Clarke, M. R., K. E. Glander, and E. L. Zucker. "Infant-Nonmother Interactions of Free-ranging Mantled Howlers (Alouatta palliata) in Costa Rica." International Journal of Primatology 19 (1998): 451-472.
Di Fiore, A. "Ranging Behavior and Foraging Ecology of Lowland Woolly Monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador." American Journal of Primatology 59 (2003): 47-66.
Fedigan, L. M., and L. M. Rose. "Interbirth Interval Variation in Three Sympatric Species of Neotropical Monkey." American Journal of Primatology 37 (1995): 9-24.
Glander, K. E. "Reproduction and Population Growth in Free-Ranging Mantled Howling Monkeys." American Journal of Physical Anthropology 53 (1980): 25-36. ——. "Dispersal Patterns in Costa Rican Mantled Howling Monkeys." International Journal of Primatology 13 (1992): 415-436.
Hartwig, W. C. "Protopithecus: Rediscovering the First Fossil Primate." History and Philosophy of the Life Sciences 17 (1995): 447-460.
Lemos de Sá, R. M., T. R. Pope, K. E. Glander, T. T. Struhsaker, and G. A. B. da Fonseca. "A Pilot Study of Genetic and Morphological Variation in the Muriqui (Brachyteles arachnoides)." Primate Conservation 11 (1990): 26-30.
Lemos de Sá, R. M., T. R. Pope, K. E. Glander, and T. T. Struhsaker. "Sexual Dimorphism in Canine Length of Woolly Spider Monkeys (Brachyteles arachnoides, E. Geoffroy 1806)." International Journal of Primatology 14 (1993): 755-763.
Milton, K. "Habitat, Diet, and Activity Patterns of Free-Ranging Woolly Spider Monkeys (Brachyteles arachnoides, E. Geoffroy, 1806)." International Journal of Primatology 5 (1984): 491-514. ——. "Mating Patterns of Woolly Spider Monkeys, Brachyteles arachnoides: Implications for Female Choice." Behavioral Ecology and Sociobiology 17 (1985): 53-59.
Moraes, P. L. R., O. Carvalho Jr., and K. B. Strier. "Population Variation in Patch and Party Size in Muriquis (Brachyteles arachnoides)." International Journal of Primatology 19 (1998): 325-337.
Nishimura, A. "Mating Behavior of Woolly Monkeys, Lagothrix lagotricha, at La Macarena, Colombia." Field Studies of New World Monkeys at La Macarena Colombia 1 (1988): 19-27. ——. "Mating Behaviors of Woolly Monkeys, Lagothrix lagotricha, at La Macarena, Colombia (III): Reproductive Parameters Viewed From a Longterm Study." Field Studies of New World Monkeys at La Macarena Colombia 7 (1992): 1-7. ——. "Social Interaction Patterns of Woolly Monkeys (Lagothrix lagotricha): A Comparison Among the Atelines. The Science and Engineering Review of Doshisha University 35 (1994): 235-254.
Peres, C. A. "Effects of Hunting on Western Amazonian Primate Communities." Biological Conservation 54 (1990): 47-59. ——. "Diet and Feeding Ecology of Gray Woolly Monkeys, Lagothrix lagotricha cana) in Central Amazonia: Comparisons With Other Atelines. International Journal of Primatology 5 (1994): 491-514.
Pope, T. R. "The Reproductive Consequences of Male Cooperation in the Red Howler Monkey: Paternity Exclusion in Multi-male and Single-male Troops Using Genetic Markers." Behavioral Ecology and Sociobiology 27 (1990): 439-485. ——. "Reproductive Success Increases With Degree of Kinship in Cooperative Coalitions of Female Red Howler Monkeys (Alouatta seniculus)." Behavioral Ecology and Sociobiology 48 (2000): 253-267.
Rylands, A. B., H. Schneider, A. Langguth, R. A., Mittermeier, C. P. Groves, and E. Rodríguez-Luna. "An Assessment of the Diversity of New World Primates." Neotropical Primates 8, no. 2 (2000): 61-93.
Stevenson, P. R. "Diet of Woolly Monkeys (Lagothrix lagotricha) at La Macarena, Colombia." Field Studies of New World Monkeys at La Macarena Colombia 6 (1992): 3-14.
Stevenson, P. R., M. J. Quiñones, and J. A. Ahumada. "Ecological Strategies of Woolly Monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia." American Journal of Primatology 32 (1994): 123-140. ——. "Influence of Fruit Availability on Ecological Overlap Among Four Neotropical Primates at Tinigua National Park, Colombia." Biotropica 32, no. 3 (2000): 533-544.
Strier, K. B., and T. E. Ziegler. "Behavioral and Endocrine Characteristics of the Reproductive Cycle in Wild Muriqui Monkeys, Brachyteles arachnoides." American Journal of Primatology 42 (1997): 299-310.
Symington, M. M. "Sex Ratio and Maternal Rank in Wild Spider Monkeys: When Daughters Disperse." Behavioral Ecology and Sociobiology 20 (1987): 333-335. ——. "Fission-Fusion Social Organization in Ateles and Pan." International Journal of Primatology 11 (1990): 47-61.
[Article by: Karen B. Strier, PhD]
