Cebus apella

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Taxonomy [top]

Kingdom Phylum Class Order Family
ANIMALIA CHORDATA MAMMALIA PRIMATES CEBIDAE

Scientific Name: Cebus apella
Species Authority: (Linnaeus, 1758)
Infra-specific Taxa Assessed:
Common Name(s):
English Guianan/margarita Island Brown Capuchin, Black-capped Capuchin, Margarita Island Capuchin
Taxonomic Notes: Silva Jr (2001, 2002) argued that the tufted capuchins and the untufted capuchins (sensu Hershkovitz 1949, 1955) are so distinct in their morphology that they should be considered separate genera. Cebus Erxleben, 1777 for the untufted group, and Sapajus Kerr, 1792 is the name available for the tufted capuchins.

Taxonomic studies have been carried out by Torres de Assumpção (1983; Torres 1988). Taxonomy of the tufted capuchins (sensu Hershkovitz 1949, 1955) here follows Silva Jr (2001), who did not recognize any subspecific forms. Groves (2001, 2005) presented an alternative taxonomy for the tufted capuchins as follows: C. apella apella (Linnaeus, 1758); C. apella fatuellus (Linnaeus, 1766); C. apella macrocephalus Spix, 1823; C. apella peruanus Thomas, 1901; C. apella tocantinus Lönnberg, 1939; C. apella margaritae Hollister, 1914; C. libidinosus libidinosus Spix, 1823; C. libidinosus pallidus Gray, 1866; C. libidinosus paraguayanus Fischer, 1829; C. libidinosus juruanus Lönnberg, 1939; C. nigritus nigritus (Goldfuss, 1809); C. nigritus robustus Kuhl, 1820; C. nigritus cucullatus Spix, 1823; C. xanthosternos Wied-Neuwied, 1826 (see Fragaszy et al. 2004; Rylands et al. 2005).

Groves (2001) and Silva Jr. (2001) differ in their definitions of the forms Cebus apella (Linnaeus, 1758) and Cebus macrocephalus Spix, 1823. Cebus apella fatuellus (Linnaeus, 1766), C. apella peruanus Thomas, 1901, and C. libidinosus juruanus Lönnberg, 1939 recognized by Groves (2001) are considered junior synonyms of C. macrocephalus by Silva Jr. (2001). C. apella tocantinus Lönnberg, 1939 recognized by Groves (2001) is considered a junior synonym of C. apella by Silva Jr. (2001).

Whereas all other tufted capuchins are considered species (following Silva Jr., 2001), the taxonomic status of the Margarita Island Capuchin has still to be reviewed. Silva Jr. (2001) did not examine specimens from the Island of Margarita, Venezuela. Groves (2001; see also Linares 1998) supposed that it was introduced in Pre-Columbian times, and found it to be more closely allied to C. a. fatuellus than with C. a. apella. Note that C. a. fatuellus is recognized as a valid subspecies by Groves, but considered by Silva Jr (2001) to be a junior synonym of C. macrocephalus.

Assessment Information [top]

Red List Category & Criteria: Least Concern ver 3.1
Year Published: 2008
Date Assessed: 2008-06-30
Assessor(s): Rylands, A.B., Boubli, J.-P., Mittermeier, R.A., Wallace, R.B. & Ceballos-Mago, N.
Reviewer(s): Mittermeier, R.A., Rylands, A.B. (Primate Red List Authority) & Hoffmann, M. (Global Mammal Assessment Team)
Justification:
Listed as Least Concern as the species is widespread and there are currently no major threats resulting in a significant overall population decline that would warrant listing in a threatened category or listing as NT. Although declines need to be considered over a period of 45 years (three generations), the species is more of a habitat generalist than other species with similar life-histories. However, it is declining in some parts of its range, including southern Pará state, Tocantins state, and northern Mato Grosso.
History:
2003 Least Concern (IUCN 2003)
2003 Least Concern

Geographic Range [top]

Range Description:Cebus apella apella
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).
Countries:
Native:
Brazil (Amapá, Amazonas, Maranhão, Pará, Rondônia, Roraima, Tocantins); French Guiana; Guyana; Suriname; Venezuela, Bolivarian Republic of
Range Map:Click here to open the map viewer and explore range.

Population [top]

Population: The nominate subspecies is widespread and common.

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: Decreasing

Habitat and Ecology [top]

Habitat and Ecology: Tropical lowland and submontane and montane rain forest, seasonally inundated forest, mangroves and savanna forests. Cebus apella inhabits a wide variety of vegetation types in Suriname and is probably more flexible in choice of habitat than any other primate species in the Guianas. It is common in high rain forest, low rain forest, riverbank high forest, mountain savanna forest, liana forest marsh forest (including Mora forest), swamp forest (including Euterpe Symphonia swamp forest and Mauritia flexuosa open swamp forest), swamp woodland (including Erythrina glaucaand Pterocarpus Tabebuia associations) and various secondary formations, and also has been reported from high forest and white sand savanna forest, savanna scrub, ridge forest (littoral woodland) and mangrove forest (Avicennia) along the coast (Mittermeier 1977; Mittermeier and van Roosmalen 1981). In Guyana, it is one of the species most often encountered along rivers (Muckenhirn et al. 1976). Arboreal quadrupeds, they are typically found in the lower to mid-canopy and understory (Freese and Oppenheimer 1981; Fragaszy et al. 2004; Jack 2007).

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

Threats [top]

Major Threat(s): Cebus apella apella
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.

Conservation Actions [top]

Conservation Actions: This species is listed on CITES Appendix II.
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.

Bibliography [top]

Aquino, R. and Encarnación, F. 1994. Primates of Peru / Los Primates del Perú. Primate Report 40: 1-127.

Bodini, R. 1989. Distribución geográfica y conservación de primates no humanos em Colombia. In: C. J. Saavedra, R. A. Mittermeier and I. B. Santos (eds), La Primatología en Latinoamérica, pp. 101-113. World Wildlife Fund - US, Washington, DC, USA.

Bodini, R. and Pérez-Hernández, R. 1987. Distribution of the species and subspecies of cebids in Venezuela. Fieldiana: Zoology 39: 231–244.

Boher-Bentti, S. and Cordero-Rodríguez, G. A. 2000. Distribution of brown capuchin monkeys (Cebus apella) in Venezuela: A piece of the puzzle. Neotropical Primates 8(4): 152-153.

Fernandes, M. E. B. 1991. Tool use and predation of oysters (Crassostrea rhizophorus) by the tufted capuchin Cebus apella apella, in brackish water mangrove swamp. Primates 32(4): 529-531.

Fragaszy, D. M., Visalberghi, E. and Fedigan, L. 2004. The Complete Capuchin: The Biology of the Genus Cebus. Cambridge University Press, Cambridge, UK.

Freese, C. H. and Oppenheimer, J. R. 1981. The capuchin monkeys, Cebus. In: A. F. Coimbra-Filho and R. A. Mittermeier (eds), The Ecology and Behavior of Neotropical Primates, Vol. 1., pp. 331-390. Academia Brasileira de Ciências, Rio de Janeiro, Brazil.

Groves, C. P. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, DC, USA.

Groves, C. P. 2005. Order Primates. In: D. E. Wilson and D. M. Reeder (eds), Mammal Species of the World, pp. 111-184. The Johns Hopkins University Press, Baltimore, Maryland, USA.

Hershkovitz, P. 1949. Mammals of northern Colombia. Preliminary report No. 4: Monkeys (Primates) with taxonomic revisions of some forms. Proceedings of the United States National Museum 98: 323–427.

Hershkovitz, P. 1955. Notes on the American monkeys of the genus Cebus. Journal of Mammalogy 36: 449–452.

Hill, W. C. O. 1960. Primates Comparative Anatomy and Taxonomy IV. Cebidae Part A. Edinburgh University Press, Edinburgh, Scotland.

IUCN. 2008. 2008 IUCN Red List of Threatened Species. Available at: http://www.iucnredlist.org. (Accessed: 5 October 2008).

Izawa, K. 1979. Foods and feeding behavior of wild black-capped capuchin (Cebus apella). Primates 20(1): 57-76.

Jack, K. 2007. The cebines: toward an explanation of variable social structure. In: C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger and S. K. Bearder (eds), Primates in Perspective, pp. 107-123. Oxford University Press, Oxford, UK.

Kinzey, W. G. 1982. Distribution of primates and forest refuges. In: G. T. Prance (ed.), Biological Diversification in the Tropics, pp. 455-482. Columbia University Press, New York, USA.

Linares, O. J. 1998. Mamíferos de Venezuela. Sociedad Conservacionista Audubon de Venezuela, Caracas, Venezuela.

Márquez, L. and Sanz, V. 1991. Evalución de la presencia de Cebus apella margaritae (Hoillister, 1914) en la Isla de Margarita. Universidad Central de Venezuela, Caracas, Venezuela.

Martinez, R. A, Moscarella, R. A., Aguilera, M. and Marquez, E. 2000. Update on the status of the Margarita Island capuchin, Cebus apella margaritae. Neotropical Primates 8(1): 34-35.

Mittermeier, R. A. 1977. Distribution, Synecology, and Conservation of Surinam Monkeys. Ph.D. Thesis, Harvard University.

Mittermeier, R. A. and Van Roosmalen, M. G. M. 1981. Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatologica 36: 1–39.

Muckenhirn, N. A., Mortensen, S., Vessey, S., Fraser, C. E. O. and Singh, B. 1975. Report on a Primate Survey in Guyana. Pan American Health Organization, Washington, DC, USA.

Norconk, M. A., Sussman, R. W. and Phillips-Conroy, J. 1996. Primates of Guayana Shield forests: Venezuela and the Guianas. In: M. A. Norconk, A. L. Rosenberger and P. A. Garber (eds), Adaptive Radiations of Neotropical Primates, pp. 69-83. Plenum Press, New York, USA.

Rylands, A. B, Kierulff, M. C. M. and Mittermeier, R. A. 2005. Some notes on the taxonomy and distributions of the tufted capuchin monkeys (Cebus, Cebidae) of South America. Lundiana 6: 97–110.

Sanz, V. and Márquez, L. 1994. Conservación del mono capuchino de Margarita (Cebus apella margaritae) en la Isla de Margarita, Venezuela. Neotropical Primates 2(2): 5-8.

Silva Jr., J. de S. 2001. Especiação nos macacos-prego e caiararas, gênero Cebus Erxleben, 1777 (Primates, Cebidae). Doctoral Thesis, Universidade Federal do Rio de Janeiro.

Silva Jr., J. de S. 2002. Sistemática dos macacos –prego e caiararas, gênero Cebus Erxleben, 1777 (Primates, Cebidae). Livro de Resumos, X Congresso Brasieliero de Primatologia: Amazônia – A Última Fronteira: 35. Bélém, Brazil.

Spironello, W. R. 1991. Importância dos frutos de palmeiras (Palmae) na dieta de um grupo de Cebus apella (Cebidae, Primates) na Amazônia Central. In: A. B. Rylands and A. T. Bernardes (eds), A Primatologia no Brasil – 3, pp. 285–296. Belo Horizonte, Brazil.

Spironello, W. R. 2001. The brown capuchin monkey (Cebus apella). Ecology and home range requirements in Central Amazonia. Yale University Press,, New Haven, CT, USA.

Terborgh, J. 1983. Five New World Primates: A Study in Comparative Ecology. Princeton University Press, Princeton, NJ, USA.

Torres, C. 1988. Resultados preliminares de reavaliação das raças do macaco-prego Cebus apella (Primates: Cebidae). Revista Nordestina de Biologia 6: 15-28.

Torres de Assumpção, C. 1983. An ecological study of the primates of southeastern Brazil, with a reappraisal of Cebus apella races. Doctoral Thesis, University of Edinburgh.

Zhang, S.-Y. 1994. Utilisation de l’espace, stratégies alimentaires et role dans la dissémination deas graines du singe capucin, Cebus apella (Cebidae, Primates), en Guyane Française. Thèse de Doctorat, Université de Paris VI.

Zhang, S.-Y. 1995. Activity and ranging patterns in relation to fruit utilization by brown capuchins (Cebus apella) in French Guiana. International Journal of Primatology 16(3): 489–507.

Zhang, S.-Y. 1995. Sleeping habits of brown capuchin monkeys (Cebus apella) in French Guiana. American Journal of Primatology 36: 327–335.

Zhang, S.-Y. and Wang, L.-X. 1995. Comparison of three fruit census methods in French Guiana. Journal of Tropical Ecology 11: 281–294.

Zhang, S.-Y. and Wang, L.-X. 1995. Fruit consumption and seed dispersal of Ziziphus cinnamomum (Rhamnaceae) by two sympatric primates (Cebus apella and Ateles paniscus) in French Guiana. Biotropica 27(3): 397–401.


Citation: Rylands, A.B., Boubli, J.-P., Mittermeier, R.A., Wallace, R.B. & Ceballos-Mago, N. 2008. Cebus apella. In: The IUCN Red List of Threatened Species. Version 2014.2. <www.iucnredlist.org>. Downloaded on 25 July 2014.
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