Overview
Distribution
Range Description
This is a wide ranging subspecies in the lower Amazon. The definition of Cebus apella apella of course determines the geographic range. As this is still controversial, the geographic range is correspondingly uncertain. Here we follow the taxonomy and proposed distributions of Silva Jr (2001). The taxonomic arrangement proposed by Groves (2001) was discussed by Rylands et al. (2005), especially in relation to the work of Torres de Assumpção (1983). It was not possible to delimit the ranges of the subspecies he recognized, but those of the species were mapped in Fragaszy et al. (2004). The one exception is in the lack of precision in the ranges of C. libidinosus and C. apella. Groves (2001) recognized C. libidinosus juruanus as the form occurring from the upper Juruá (type locality: Brazil: Frente a João Pessôa, Rio Juruá) extending east in a swathe through northern Mato Grosso. In the map provided in Fragaszy et al. (2004), C. libidinosus juruanus is restricted to the upper Juruá (a range proposed by Hill [1960]), and entirely surrounded by C. apella, which of course is unreasonable: it should have a range which is contiguous with other C. libidinosus subspecies. If a valid taxon, the range of C. l. juruanus should extend through northern Mato Grosso to meet the range C. l. libidinosus, but its limits are unclear. The requirements for any conservation assessment and subsequent conservation action are that the taxon is defined and its geographic distribution delineated. Silva Jr. (2001) provided a taxonomy and distribution maps. This in no way discards the taxonomy proposed by Groves (2001). Further research is needed.
The range of Cebus apella apella described here includes that of C. apella tocantinus Lönnberg, 1939, from the south of the lower to middle Amazon, Cebus libidinosus pallidus Gray, 1866 from the central and northern Bolivia (as indicated by Groves 2001), part of the range of C. macrocephalus Spix, 1823 (lower to middle Amazon north of the Rio Amazonas), and the part of that of C. libidinosus juruanus that Groves (2001) proposed extended through Rondônia to northern Mato Grosso.
The stronghold of the type species is the Guianas, and Brazil, at least east of the Rio Negro. Boher-Bentti and Cordero-Rodríguez (2000) extended it to the southern extreme of the Orinoco Delta, although it is otherwise not recognized as occurring in eastern Venezuela (Bodini and Pérez-Hernández 1987; Linares 1998). In Venezuela, it occurs in the Federal Territory of Amazonas, along both sides of the upper Rio Orinoco, its precise range being limited by savannas. The range to the west is constrained by C. macrocephalus and to the south by C. libidinosus. In the east to the interfluvium of the rios Itapecuru and Parnaiba in the state of Maranhão. In Bolivia, Cebus apella occurs south of the Madre de Dios, south to the headwaters of the ríos Mamoré and Beni, where it meets the range of C. cay occurring in southern Bolivia, the Brazilian Mato Grosso, Paraguay and Argentina. It extends into south-east Peru along the south of the Río Madre de Dios, west as far the Rio Inambari (recognized as C. a. pallidus by Aquino and Encarnación [1994]). In the southern Amazon, C. apella would be restricted by the transition to Cerrado, the bush savanna of central Brazil where C. libidinosus occurs.
Cebus apella margaritae
Cebus apella margaritae lives in four forest fragments on the east side of Margarita Island in Venezuela: El Copey Nacional Park (7,130 ha) rising to 930 m above sea level; the Serranía of Cerro Tragaplata (~4,400 ha) an unprotected area rising to 680 m above seas level; Cerro Matasiete Natural Monument (1,145 ha) rising to 660 m asl; and Cerro Taguantar (~1,000 ha) an unprotected area rising to 520 m above sea level. Monkeys were reported in Cerro Taguantar in 2007 (Ceballos-Mago, direct observation).
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Geographic Range
Cebus apella is found east of the Andes from Colombia and Venezuela to Paraguay and northern Argentina.
Biogeographic Regions: neotropical (Native )
- Emmons, L. 1990. Neotropical Rainforest Mammals. Chicago and London: The University of Chicago Press.
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Physical Description
Morphology
Physical Description
Brown capuchin monkeys vary in color from light brown to mustard yellow to black. The shoulders and underbelly are lighter than the rest of the body. There is a patch of coarse black fur on the crown of the head, sometimes referred to as a cap. Above the ears the black hairs form tufts of fur giving the species one of its common names, tufted capuchin monkey. Facial patterns are variable among individuals, but black sideburns extending from the cap are characteristic of Cebus apella. The hands, feet, and tail are either black or dark brown.
The tail is long and prehensile. Cebus apella is the only species of capuchin monkey known to carry its tail in a tight coil.
This species is robust and stocky. Brown capuchin monkeys have a deep lower jaw and large jaw muscles to accomodate a diet of large fruits and rough vegetation. Males are 34% larger in body size and have canines 22% larger than those of females.
Range mass: 1300 to 4800 g.
Other Physical Features: endothermic ; homoiothermic; bilateral symmetry
Sexual Dimorphism: male larger
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Ecology
Habitat
Habitat and Ecology
Capuchins are frugivores-insectivores, including wide variety of fruits, seeds and arthropods, frogs, nestlings and even small mammals, supplemented by stems, flowers and leaves. They are extractive, manipulative foragers (see Izawa 1979; Fernandes 1991). Largely sympatric with the untufted capuchins, eitherCebus olivaceus or C. albifrons. The species differ most markedly in their diet through their use of palm fruits (Terborgh 1983; Spironello 1991, 2001). Mean group size for Cebus apella is 18 individuals, with numbers of females exceeding the numbers of males (adult sex ratio of 0.85). Males disperse. Both sexes take up linear hierarchies, the top ranking male being dominant to the top ranking female. Subordinate males are often peripheral (Fragaszy et al. 2004). Zhang (1994, 1995a,b; Zhang and Wang 1995a,b) carried out a field study of the ecology and behaviour of this species in French Guiana.
In the Guianas, C. apella group sizes usually range from 10-20 animals (Mittermeier 1977; Spironello 1991; Zhang 1995b). Groups sometimes split into subgroups and forage on their own in different directions. The home range of the best known group in the Voltzberg site of Mittermeier (1977) was roughly 146 ha, and a second group, which ranged outside as well, covered 62 ha of his study area. Larger home ranges have been recorded by Zhang (1995b) in French Guiana (approximately 355 ha) and by Spironello (2001) north of Manaus in Brazil (around 900 ha).
Size: Adult male 1.35-4.8 kg (mean 3.05 kg); adult female: 1.76-3.4 kg (mean 2.4 kg) (Jack 2007).
Cebus apella margaritae
The vegetation cover of the mountains inhabit by Margarita Island Capuchins have particular ecological interest, because they support an isolated cloud forest at an exceptionally low altitude (ca. 600 m above sea level) contrasting with an arid lowland (Sugden 1986). Home range is about 78 ha (Márquez and Sanz 1991; Sanz and Márquez 1994). The diet is comprised of fruits, insects, flowers, leaves, seeds and piths. Margarita Island Capuchins are particularly shy and cryptic, avoiding human contact probably due to the hunting pressure.
Systems
- Terrestrial
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Habitat
Cebus apella inhabits moist subtropical or tropical forests, but has also been seen in dry forest, gallery forest, disturbed and secondary forest. In northwest Argentina these monkeys live in montane forest at an elevation of 200 to 1100m. This species prefers the understory and midcanopy of the forest, but often descends from the trees to forage and play. Cebus apella has the widest range and broadest habitat tolerances of any other Cebus species.
Range elevation: 1100 (high) m.
Habitat Regions: tropical ; terrestrial
Terrestrial Biomes: forest ; rainforest ; mountains
- Kinzey, W. 1989. New World Primates: Ecology, Evolution, and Behavior. New York: Aldine De Gruyter.
- Nowak, R. 1991. Walker's Mammals of the World, Fifth Edition. Baltimore and London: The Johns Hopkins University Press.
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Trophic Strategy
Food Habits
Fruits are a large part of brown capuchin monkey's diet. This species can eat larger fruits than other species of capuchin monkey because of their robust jaws. Vegetation, seeds, pith, eggs, insects, reptiles, birds, and small mammals (such as mouse opossums) are also included in their diet. During the dry season, when food is scarce, Scheelea palm frond pith is critical to this animal's survival.
Foraging is a noisy and destructive activity. Brown capuchin monkeys move from tree to tree, ripping apart vegetation and cracking open nuts against branches. They look for vertebrate and invertebrate prey by destroying dead vegetation and capturing anything inside. Individuals who catch prey do not usually share with other group members.
Animal Foods: birds; mammals; amphibians; reptiles; eggs; carrion ; insects; terrestrial non-insect arthropods
Plant Foods: leaves; roots and tubers; wood, bark, or stems; seeds, grains, and nuts; fruit; flowers
Primary Diet: omnivore
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Associations
Ecosystem Roles
Brown capuchin monkeys are important predators on small animals and may disperse the seeds of some forest plants when they eat the fruit.
Cebus apella can be found in mixed species groups. They are most often found in association with squirrel monkeys (Saimiri sp.). Usually the squirrel monkeys initiate the mixed group interaction, probably in order to find food more efficiently. Squirrel monkeys follow brown capuchin monkeys to new food sources, which saves them foraging time. The association does not seem to benefit capuchin monkeys.
Ecosystem Impact: disperses seeds
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Predation
The dominant male protects his troop from predators by sounding alarm calls. This draws attention to himself so that his troop can escape. Capuchin monkeys are very wary of predators.
Members of a troop give sharp whistling calls at the sight of hawks and eagles, two of the most significant predators of this species. The troop is so wary of hawks and eagles that it sounds alarm whistles even if the bird flying overhead is harmless.
Known Predators:
- hawks and eagles (Accipitridae)
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Life History and Behavior
Behavior
Communication and Perception
These monkeys scent mark themselves by washing their hands in their own urine and rubbing their hands on their fur. This may be a way for males to advertise their sexual maturity.
Female brown capuchin monkeys in estrus try to attract the attention of the dominant male by following him and making loud calls. A wide variety of vocalizations is known from Cebus species. These were divided into 4 categories in C. olivaceus: contacting the group, contacting individuals, ending aggressive encounters, alerting the group to the presence of danger.
Gestures and facial expressions are also widely used in communication and social grooming is an important form of contact.
Communication Channels: visual ; tactile ; acoustic ; chemical
Other Communication Modes: pheromones ; scent marks
Perception Channels: visual ; acoustic
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Life Expectancy
Lifespan/Longevity
Typical longevity in the wild is unknown, but captive C. apella may live to 45 years old.
Range lifespan
Status: captivity: 45 (high) years.
Average lifespan
Status: captivity: 44.6 years.
Average lifespan
Sex: male
Status: captivity: 41.0 years.
Average lifespan
Status: wild: 40.0 years.
Average lifespan
Sex: male
Status: captivity: 45.1 years.
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Lifespan, longevity, and ageing
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Reproduction
Reproduction
Cebus apella has a polygamous mating system. Females mate preferentially with the dominant male. Other males have mating opportunities when the dominant male is not present. During the last two days of a female's estrus cycle, the dominant male is very protective and keeps the female from mating with subordinate males.
Mating System: polygynous
Cebus apella does not appear to have a breeding season, though most births may occur during the dry season or early rainy season. The ovarian cycle lasts for approximately 21 days and female's show no external genital swellings during estrus. The gestation period is 150-160 days and one infant is born, twins are very rare.
Young males leave their natal group once they reach sexual maturity. Male brown capuchin monkeys are considered sexually mature at 7 years of age. Females mature earlier and may give birth to their first offspring as early as 4 years old.
Breeding interval: Capuchins give birth once yearly.
Breeding season: Births and breeding may occur in any season, but may be more frequent during dry or early rainy seasons.
Range number of offspring: 2 (high) .
Average number of offspring: 1.
Range gestation period: 150 to 160 days.
Average age at sexual or reproductive maturity (female): 4 years.
Average age at sexual or reproductive maturity (male): 7 years.
Key Reproductive Features: iteroparous ; year-round breeding ; gonochoric/gonochoristic/dioecious (sexes separate); viviparous
Average birth mass: 239.7 g.
Average number of offspring: 1.5.
Average age at sexual or reproductive maturity (female)
Sex: female: 1703 days.
Parenting is left to the females, although males are tolerant of juveniles. Allomothering is a common practice. Infant capuchin monkeys cling to their mothers fur during their first few months of life. Mothers travel with their infants and nurse them during that time. If a young capuchin monkey is separated from its mother, other members of the troop will respond to the infant's distress calls. Female capuchins remain in their natal group at adulthood while males disperse.
Parental Investment: altricial ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Provisioning: Female, Protecting: Female); pre-weaning/fledging (Provisioning: Female, Protecting: Male, Female); pre-independence (Provisioning: Female, Protecting: Male, Female); post-independence association with parents; extended period of juvenile learning
- Emmons, L. 1990. Neotropical Rainforest Mammals. Chicago and London: The University of Chicago Press.
- Kinzey, W. 1989. New World Primates: Ecology, Evolution, and Behavior. New York: Aldine De Gruyter.
- Linn, G. 1995. American Journal of Primatology.
- Nowak, R. 1991. Walker's Mammals of the World, Fifth Edition. Baltimore and London: The Johns Hopkins University Press.
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Molecular Biology and Genetics
Molecular Biology
Barcode data: Cebus apella
There are 3 barcode sequences available from BOLD and GenBank. Below is a sequence of the barcode region Cytochrome oxidase subunit 1 (COI or COX1) from a member of the species. See the BOLD taxonomy browser for more complete information about this specimen and other sequences.
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Download FASTA File
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Statistics of barcoding coverage: Cebus apella
Public Records: 3
Species: 4
Species With Barcodes: 1
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Conservation
Conservation Status
IUCN Red List Assessment
Red List Category
Red List Criteria
Version
Year Assessed
Assessor/s
Reviewer/s
Contributor/s
Justification
History
- 2003Least Concern(IUCN 2003)
- 2000Lower Risk/least concern
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Conservation Status
Because of its high reproductive potential and its habitat flexibility, hunting and habitat destruction have not devastated populations as severely as they have other species of primates. However, certain subspecies may be threatened, including C. a. xanthosternos and C. a. robustus from the Atlantic forests of eastern Brazil.
Cebus apella is the most commonly seen monkey in Amazonia.
US Federal List: no special status
CITES: appendix ii
IUCN Red List of Threatened Species: least concern
- Rylands, A., R. Mittermeier, E. Rodriguez-Luna. 1997. Conservation of Neotropical Primates: Threatened Species and an Analysis of Primate Diversity by Country and Region. Folia Primatologica, 68: 134-160.
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Trends
Population
Population density of the Margarita Island Capuchin has not been properly estimated yet. Results of an ongoing project about ecology and conservation of the Margarita Island Capuchin will allow the determination of densities in the near future. According to Sanz and Marquez (1994), total population is only 250-300 animals. Marquez and Sanz (1991) estimated between 0.02 and 0.23 groups/hours of observation in different forest fragments. Group size was 4.5 ind/group in average. During surveys conducted in 2007, group size varied between 2 and 15 individuals (N. Ceballos-Mago, direct observation).
Population Trend
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Threats
Threats
The Guianan tufted capuchin is hunted for food and as pets (this is the most common primate kept as pets), but is an adaptable species.
Cebus apella margaritae
Although part of the distribution of the Margarita Island Capuchins is within protected areas (Cerro el Copey National Park and Cerro Matasiete Natural Monument), they are still threatened by hunting pressure and by habitat loss and fragmentation. Habitat fragmentation on Margarita Island is mainly caused by road construction and growth of towns. Sanz and Marquez (1994) considered that hunting pressure for pest control could be the main factor driving this subspecies to extinction in a few years. Currently, hunting pressure for pest control has been reduced only in the Cerro el Copey National Park. Capture of monkeys for pet trade in the whole distribution area of the monkeys has increased and can be currently one of the most important threats (Ceballos-Mago direct observation). Preliminary results of surveys have revealed an important national and international illegal traffic of primates. Release of monkey pets in the habitat of the Margarita Island Capuchin is another threat for these primates (Martinez et al. 2000). Such releases must be considered in terms of the level of risk of disease transmission and hybridization.
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Management
Conservation Actions
Cebus apella apella occurs in numerous protected areas, many of which are very large.
Brazil
Tumucumaque National Park (3,882,376 ha)
Cabo Orange National Park (630,017 ha)
Gurupí Biological Reserve (272,379 ha)
Lago Piratuba Biological Reserve (394,223 ha)
Rio Trombetas Biological Reserve (409,578 ha)
Uatumã Biological Reserve (942,786 ha)
Jari Ecological Station (207,370 ha)
Terra do Meio Ecological Station (3,373,111 ha)
Niquia Ecological Station (282,803 ha)
French Guiana
Parc amazonien de Guyane (3,300,000 ha)
Nouragues Natural Reserve (100,000a)
La Trinité Natural Reserve
Kaw Reserved Area (76,800 ha)
Guyana
Kaietur National Park (11,655 ha)
Iwokrama Forest Reserve (364,000 ha)
Suriname
Brinckheuvel Nature Reserve (6,000 ha) (probable: Mittermeier and van Roosmalen 1982)
Central Suriname Nature Reserve (1,600,000 ha) (Mittermeier and van Roosmalen 1982)
Coppename Monding Nature Reserve (12,000 ha) (probable: Mittermeier and van Roosmalen 1982)
Galibi Nature Reserve (100 ha) (Mittermeier and van Roosmalen 1982)
Sipaliwini Nature Reserve (100,000 ha) (Mittermeier and van Roosmalen 1982)
Wia-wia Nature Reserve (36,000 ha) (Mittermeier and van Roosmalen 1982)
Brownsberg Nature Park (8,400 ha) (Mittermeier and van Roosmalen 1982; Norconk et al. 2003)
Cebus apella margaritae
Several recommendations have been proposed for the conservation of the Margarita Island capuchin (Marquez and Sanz 1991; Sanz and Marquez 1994; Martinez et al. 2000; Sanz 2001, 2003):
•To survey accurately the natural population of Cebus apella margaritae.
•To carry out population demography studies.
•To determine accurately home range and use of habitat.
•To carry out productivity studies.
•To solve the monkey-farmer conflict for crop raiding.
•To determine the presence/absence of Cebus olivaceous in the mountains.
•To control the illegal hunting and the illegal traffic of monkeys.
•To evaluate risks of zoonoses.
•To declare a protected area including the mountains in the north part of the island, in order to facilitate the movements of the monkeys between those mountains.
•To conduct environmental educational programmes.
•To conduct genetic studies
Unfortunately, most of these recommendations have not yet been implemented. The regional office of INPARQUES (National Parks Institute) about seven years ago started to plan the increase in area of the Cerro El Copey National Park, in order to include the mountains in the north and the west of the park. Nevertheless, this plan has not been executed until now. There is still a need to develop proper management strategies for the Margarita capuchin monkey and its habitat. There is an ongoing project of ecology and conservation of the Margarita Island capuchin that will generate actual information about this monkey population.
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Relevance to Humans and Ecosystems
Benefits
Economic Importance for Humans: Negative
There are no known negative affects of C. apella on humans.
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Economic Importance for Humans: Positive
Cebus apella has been extensively hunted for meat. These animals are also popular pets in many parts of the world. They have been trained to perform household tasks for people with disabilities and are most commonly known as the monkeys used by itinerant "organ grinders".
Positive Impacts: pet trade ; body parts are source of valuable material; research and education
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