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White-fronted capuchin

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White-fronted capuchin
Scientific classificationEdit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primates
Suborder: Haplorhini
Infraorder: Simiiformes
Family: Cebidae
Subfamily: Cebinae
Genus: Cebus
Groups included
Geographic range of the various white-fronted capuchin species in South America
Geographic range of the various white-fronted capuchin species in South America
Cladisticallyincluded but traditionally excluded taxa

White-fronted capuchincan refer to any of a number of species ofgracile capuchin monkeywhich used to be considered as the single speciesCebus albifrons.White-fronted capuchins are found in seven different countries inSouth America:Bolivia,Brazil,Colombia,Venezuela,Ecuador,Peru,andTrinidad and Tobago.

White-fronted capuchins are medium-sized monkeys with a light brown back and a creamy white underside. Like othercapuchin monkeys,they areomnivorous,feeding primarily onfruits,invertebrates,other plant parts and sometimes small vertebrates. They are predated upon primarily byraptorsand probably small cats, especially themargay,though snakes have been known to attack them. They arepolygamousprimates and live in fairly large groups of 15 to 35 individuals. Reproductive females give birth to a single young at biennial intervals. They maintainhome rangesof 1.2 to 1.5 km2(0.46 to 0.58 sq mi) and have complex vocal repertoires. They are among the few primates to have been observed crafting and utilising tools in the wild.

White-fronted capuchins are common and widespread, although their population may be declining.[1]The decline is believed to be caused by human-inducedhabitat lossand degradation, and hunting. In 2008 theInternational Union for Conservation of Nature(IUCN) classified theEcuadorian white-fronted capuchin(C. equatorialis) and theTrinidad white-fronted capuchin(formerly regarded asC. albifrons trinitatis) as "critically endangered," and thevaried white-fronted capuchin(Cebus versicolor) in Colombia as "endangered." The total population of the Trinidad subspecies was 61 at the last census.[citation needed]

Taxonomy

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Even when the white-fronted capuchins were all considered to belong to a single species, there were problems with its name, description and type locality. Theholotypedoes not exist; the original description byAlexander von Humboldtin 1812 describes an animal that is much darker (grayish) than those that exist close to thetype locality,and the description includes a dark tail tip, a character that is completely unknown in any population of the species.[2]Additionally, the animal which von Humboldt examined was a tame animal inMaipures,where the species is not found. The closest population is about three kilometers to the north, on the other side of theTuparro River.[3]

Defler and Hernandez established aphenotypefrom the population that was calledCebus albifrons albifronsby Hernández C. and Cooper.[3][4]Another problem has been that thetaxonC. a. unicolordescribed by Spix (1823)[5]and further defined by Hershkovitz was indistinguishable fromC. a. albinos;the two are synonymous.[6][4][3]

Taxonomic classification

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Hershkovitz (1949) originally named 13 subspecies, while Hernández-Camacho and Cooper (1976) described eight subspecies for Colombia.[4]Colin Grovesassessed the species in 2001, further reducing the number.[7]One notable subspecies outside of Colombia is the critically endangered Trinidad white-fronted capuchin. The following subspecies were recognised by assessors working for theIUCNas of 2015.[1]

  • Ecuadorian white-fronted capuchin,Cebus albifrons aequatorialis,[8]found in western Ecuador and Peru (critically endangered).
  • White-fronted capuchin,Cebus albifrons albifrons,[1]found in Bolivia, Brazil, Colombia, Peru and Venezuela.
  • Río Cesar white-fronted capuchin,Cebus albifrons cesarae,[9]found in Colombia.
  • Shock-headed capuchin,Cebus albifrons cuscinus,[10]found in Bolivia, Brazil, Ecuador and Peru.
  • Santa Marta white-fronted capuchin,Cebus albifrons malitiosus,[11]found along the northern flanks of theSierra Nevada de Santa Martain Colombia.
  • Trinidad white-fronted capuchin,Cebus albifrons trinitatis,[12]61 individuals estimated on the island ofTrinidadin 2008 (critically endangered).
  • Varied white-fronted capuchin,Cebus albifrons versicolor,[13]found in Colombia (endangered).

The IUCN list differs from that by Groves (2005) in that Groves excludedC. a. cesaraeandC. a. malitiosusbut includedC. a. unicoloras a subspecies.[14]In theHandbook of the Mammals of the World(2013)Mittermeierand Rylands limitC. albifronsto gracile capuchins found in the upper Amazon basin in southern Venezuela, southern and eastern Colombia and northwest Brazil, based largely on the work of Jean Boubli,Thomas DeflerandJorge Hernández-Camacho.[15][16]In particular, the following forms that had previously been considered subspecies or populations ofC. albifronshave been reclassified as separate species:[15]

Mittermeier and Rylands consider the Trinidad white-fronted capuchin to be synonymous with thebrown weeper capuchin(C. brunneus), but other authors including the IUCN regard it as a separate species,C. trinitatis.[17]

The difficulties in identifying separate subspecies and species have been pronounced. Hernández-Camacho and Cooper reported some specimens of capuchin from theBarranquillaanimal market had supposedly come from the middle valley of theSan Jorge River.[4][18]It is difficult to determine whether these arewhite-faced capuchins(Cebus capucinus) or white-fronted capuchins. Intermediate characteristics include a dark crown that is high and removed from the forehead. The white parts on the face are more distinctively bald and the outside parts of the arms and legs are more clear; this suggests they are white-headed capuchin.[4]Some specimens ofC. versicolorseen in the market atMagangué‚ and probably captured in the lowerCauca River,show similar tendencies to the above, except that there is no increase in the dark pigmentation. Based on these observations and on various "intermediate" specimens from northern Colombia, it is possible that an investigation of the contact zone between the white-headed capuchin and white-fronted capuchin ultimately could show that these forms areconspecific,or that some species of white-fronted capuchin are actually more closely related to white-faced capuchins than they are to other white-fronted capuchins.[4][16]Another critical zone for this analysis is an area in northeast Ecuador whereC. aecuatorialesand white-faced capuchins are found, although neithersympatricdistributions orintergradationhave as yet been determined.[4][19]

Description

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Male white-fronted capuchins usually weigh an average of 3.4 kg (7.5 lb) and the females an average of 2.9 kg (6.4 lb), although a male onMirití-Paranáin Colombia weighed 5.5 kg (12 lb).[20]This primate is usually maroon-white orpalominoand creamy white. It has short fingers and anopposable thumb.[21]Like other capuchins its premolars are large, and it has square-shaped molar with a thick enamel to help with cracking nuts.[21]Below are descriptions of the known species forColombia.

  • Humboldt's white-fronted capuchin,Cebus albifrons,is found in easternVichada,close to the type locality, and was defined by von Humboldt using a tame animal maintained by humans (and a pig) in the village of Maipures.[2]The original description of von Humboldt described an ashy gray animal with a black tail tip,[2]characteristics that are not typical of any known population of white-fronted capuchin. TheC. albifronslocated three kilometers to the north of Maipures are very light colored animals with yellowish or reddish tones, very similar to the population of Arauca.
  • Spix' white-fronted capuchin,Cebus unicolor[5]is also very light colored with yellowish tones and was once thought to be a likely synonym ofC. albifrons.[3]One population of very pallid coloration is found inArauca,the northern part ofBoyacáand the eastern part ofNorte de Santanderand probably representsC. a. albifrons.
  • The Río Cesar white-fronted capuchin,Cebus cesaraeis very light in color and quite well-defined as a subspecies. "The cap is cinnamon or snuff-brown; median dorsal region, forearm and forelag with orangeous and contrasted with sides of back and trunk; hairs of belly and chest ochracous-orange to pale ochraceous-buff and silvery; contrasting pale area of front extending over variable amounts of upper surface of shoulder and inner side of upper arm" (Hershkovitz, 1949).[6]
  • The Santa Marta white-fronted capuchin,Cebus malitiosus,is characterized by a color that is rather dark brown over almost the entire body with yellowish shoulders. "Pale area of front less extensive, upperparts and limbs paler than inhypoleucus.Cap prout's brown, median dorsal region cinnamon brown, forearm and foreleg not markedly contrasting in color with back and sides of body; hairs of belly and chest ochraceous-tawny to cinnamon-brown and silvery; contrasting pale area of front extending well over upper surface of shoulder and inner side of upper arm "[22](Hershkovitz, 1949).[6]
  • The varied white-fronted capuchin,Cebus versicolor,is acomplexwhich includes dark populations and lighter populations.[23]It includes the former subspeciesC. a. pleei.[6]and was once thought to also include the Sierra de Perijá white-fronted capuchin,C. leucocephalus.[24]Herskovitz's description ofC. a. pleeiis of a very reddish animal, particularly in its limbs while his description ofC. a. versicoloris a lighter red.[6]He describedC. a. leucocephalusas a dark brown animal with reddish tonalities in the hind legs.[6]Nevertheless, Hernández-Camacho and Cooper discussed evidence that the three subspecies (C. a. leucocephalus,C. a. pleeiandC. a. versicolor) could be subsumed into one subspecies (C. a. versicolor), since the variations seem to be found in a very well-defined zone and even in the same groups, close toBarrancabermejaon the eastern bank of the middleMagdalena Riverin theDepartment of Santander.[4]This suggested to them that the dark phase (C. a. leucocephalus) and the light phase (C. a. pleei) are extremes of an intermediate (C. a. versicolor).[4]Boubli's research suggested thatC. a. pleeimay be synonymous withC. versicolorbut was more likely synonymous withC. cesarae,which he found to be closely related toC. versicolor.[16]Boubli foundC. a. leucocephalusto be a separate species.[16]
  • The shock-headed capuchin,Cebus cuscinus,is found south of the Guamués River and colored a light brown.[6][7]

Geographic range and habitat

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White-fronted capuchins are found in a variety of forest types. InVichadait exploits a morexerichabitat in terms of drainage, compared with thetufted capuchin,which tends to be found in forests that are moremesophytic.[25]It is also found in flooded forests.[25]The white-fronted capuchin survives well in forests growing over white sand and in forests of "highcaatinga"growing in the rocks and gravel at the foot ofmesas.[25]

In Colombia, white-fronted capuchins are found from the northern slopes of theSierra de Santa Martato the south, in the valley of theMagdalena Riverto an as yet undefined point in theDepartment of Tolimaand in the valley of the lowerCauca River,to the eastern parts of centralAntioquiaand the southern parts ofSucreto the west. InGuajirathe species is found toRiohacha,and an isolated population is apparently found in theSerranía de Macuira,though this needs confirmation. They are also found along the slopes of theSerranía de Perijáand theCordillera Oriental.To the east of the Cordillera they are found inNorte de Santander,westernArauca,in easternVichadabetween theMetaand Tuparro rivers, and then south of theVichada River;although east of the Ariari River, not including the Ariari itself. It is not known whether they are found in the rather extensive forests of the upper Manacasías River inMeta.South of the Guayabero andGuaviare River,white-fronted capuchins are found throughout theAmazon.The species is known to an altitude of 1,500–2,000 m (0.93–1.24 mi) in theDepartment of Tolima.

Outside of Colombia, white-fronted capuchins are found from theAndesthroughout eastern Ecuador, Peru and northern Bolivia to theTapajósriver inBrazil,south of theAmazon River.North of the Amazon River they are found in the southern parts of the Venezuelan Federal State ofAmazonasand in northern Brazil between Colombia and theBranco River.There are isolated populations of the Ecuadorian white-fronted capuchin (C. aequatorialis) in thePacific Equatorial Forest,with at least three troops present in the premontane cloud forest and moist transitional forest of theJama-Coaque Reserve(Reserva Jama-Coaque) along the coastal equatorial mountain range in the province of Manabi, Ecuador.[26]

Humboldt's white-fronted capuchin,Cebus albifrons,is very common in the eastern half ofEl Tuparro National Park,Colombia. It is less common inAmacayacu National Park.Cebus a. yuracusis known south of thePutumayo River.Cebus versicoloris widespread on the middle-Magdalena Riverand is observable in preserved woodlots of protectedfincas.Cebus malitiosusis easy to observe inTayrona National Park,east ofSanta Marta.Cebus a. cesaraecan be located in theSerranía del Perijáeast ofValledupar,Cesaralso in Colombia.

Behavior and ecology

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White-fronted capuchins have been studied inColombiabyDefler,in two different sites inPeruby Soini and Terborgh, inTrinidadby Phillips and inEcuadorby Matthews.[27][28][29][30][25][31][32][33][34][35][36]

In eastern Vichada, Colombia, white-fronted capuchins are found in large groups of around 35 individuals, while to the south in closed forest (perhaps as a result of competition with thetufted capuchin) they have an average group size of 8–15 individuals. A group in Vichada used a home range of about 1.2 km2(0.46 sq mi),[27]while Terborgh found a home range of more than 1.50 km2(0.58 sq mi) and Matthews calculated 240 hectares (590 acres).[32][35]Near the type locality ingallery forestand islands of forest in Vichada, they have an ecological density of around 30 individuals/km2.[27]In forests with closed-canopy in Colombia and in southern Vichada, many areas have very low densities. Around the lowerApaporis River,for example, densities are less than one individual/km2and the size of the groups is around 15 individuals. Low densities in many parts of the Colombian Amazon make it difficult to detect the presence of the species in many parts.

Terborgh found an average of 1,800 metres (1.1 mi) for the day range of a group, and calculated the following time budget of the study group inManú National Park,Peru: 18% rest, 21% travel, 22% feeding on plant material and 39% feeding on insects; total feeding 61%.[32]Matthews however, registered 54% foraging, 25% moving and 21% feeding and socializing.[35]They are primarilyquadrupedal,although they utilize a great variety of gallops, jumps, falls and climbing. During certain times of the year they are extremely terrestrial, especially when there is a scarcity of available fruits and the troop must search forarthropodsin the dry leaves of the forest floor. In some parts of theLlanos Orientalesthey are found walking over the grassysavannabetween forests, leaving well-beaten trails. In Vichada it uses preferential trees for sleeping at heights of 25–30 metres (82–98 ft). The palmAttalea regiais often used for sleeping in this zone.

Diet

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All species of capuchin tend to have a rather similar diet in broad terms; they are omnivores, eating fruits and small invertebrates, small vertebrates and birds' eggs, which they forage at all levels of the forest, frequently descending to the forest floor. In northern Colombia during the dry season when there are few fruits to be found, white-fronted capuchins spend more than half their time on the ground, searching for and capturing smallprey.They are extremely good at manipulating objects, and spend a great deal of time examining dry leaves from which they collect invertebrates (for example smallbeetlesandants' eggs) from rolled up leaves. They huntfrogsand drink the water which accumulates in the spaces between the bracteoles of the common plantPhenakospermumguianense,where the frogs hide. Huntingamphibiansseems to be a cultural phenomenon which the members of each group learn.P. guianenseis commonly present in large, dense stands in some types of forest.

In Manú National Park the animal material in the diet includes frogs,lizards,small mammals and birds' eggs as well as many invertebrates, includingorthopterans,lepidopteransandhymenopterans(especially ants andwasplarvae). In thePacaya–Samiria National Reservation,they have been observed eatingtent caterpillars.[37]Terborgh identified 73 species of plants from 33 families consumed by this primate.[32]TheMoraceaewas the most important family by a wide margin, counting the number of species (17) eaten, equivalent to 23.3% of all plant species consumed. Importance values for plant families consumed by the white-fronted capuchin in one study are as follows: Moraceae (17, 23.3%);Leguminosae(5, 6.8%);Araceae(4, 5.5%);Bombacaceae(4, 5.5%);Palmae(4, 5.5%).[32]

Defler collected 40 species of plants from 23 families eaten by white-fronted capuchins in Vichada according to species consumed per family:Arecaceae(7);Moraceae(6);Chrysobalanaceae(3);Leguminosae(3);Passifloraceae(2);Bromeliaceae(2);Burseraceae(2);Bombacaceae(1);Celastraceae(1);Connaraceae(1);Euphorbiaceae(1);Lecythidaceae(1);Maranthaceae(1);Melastomataceae(1);Anacardiaceae(1);Myrtaceae(1);Annonaceae(1);Musaceae(1);Apocynaceae(1);Orchidaceae(1);Araceae(1);Rubiaceae(1);Bignoriaceae(1).[27]

In terms of importance value, palms are highly valued by all species of capuchin. InEl TuparroNational Park in Colombia, the palmAttalea regiaewas a key species for white-fronted capuchins, the nuts being a principal food.[27]In Manú National Park in Peru the palmsAstrocaryumandAttaleawere the most important palm genera, but perhaps not at the same level asAttaleain El Tuparro. Also, at Manú various species ofFicuswere very important to white-fronted capuchins; this emphasis onFicuswas not observed in the El Tuparro study, although this study did not include an entire year. Nevertheless, research on other species suggests the importance of palms as "key species" and the lack of importance ofFicusin such habitats as gallery forests in the llanos of Colombia and Venezuela, contrasts with their high importance in more fertile habitats like Manú.

White-fronted capuchins take advantage of almost any water source, drinking water from tree holes when available, but also drinking from brooks and springs when necessary. During the driest season in Vichada the group studied by Defler went to the ground every day to a water seep from under a huge boulder, which was the only water source available in their home range.[27][28]

Reproduction

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Humboldt's white-fronted capuchin and baby

White-fronted capuchins are polygamous. The male mounts the female, holding her legs with his hind feet, and copulates with her for a few minutes. Although the time ofgestationis unknown, it is probably around 160 days like the tufted capuchin. Usually one infant is born. Observations of a newborn in El Tuparro National Park showed the process by which the newborn discovered the appropriate position for riding on the mother. Newborns ride oriented sideways over the mothers' shoulders, but during the first days the baby holds on to any part of the mother such as the base of the tail, the tail, the legs, and the arms before discovering and learning that the position over the shoulders is best and most secure. After several weeks the baby makes the change from the sideways position over the shoulders to riding on her back.

All the members of the troop are interested in the newborn, and they take advantage of any opportunity to examine and look at its genitals if the mother permits it. With time the baby begins to climb up on other members of the troop, including the adult males who are interested in protecting the little one. Playing behavior is principally with a companion, and all members of the troop from the alpha male, the mother and all young members of the group solicit play with the young one.

Social structure

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Adult males are notably tolerant of each other in the group, but they are very aggressive towards males of other groups. Defler observed intergroup aggressive behavior among Humboldt's white-fronted capuchins in El Tuparro, which resulted in one group fleeing towards the central parts of their territory.[28][15]Alpha males seem to exercise a "control position" at the center of the group, since all members are extremely conscious and alert to his location, and they all observe his reactions. If the alpha reacts with intense fear or panic or if he pays close attention to something, all members of the troop react similarly. The presence of adult males seems to lend psychological support to the smaller adult females. Defler noticed that more timid females often became quite aggressive towards him when a male appeared on the scene, although the females often needed to press up against the flank of the male for reassurance.[28]

Communication

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Vocalizations are variable, and some are listed as follows:[28](1) ua – a soft bark given repeatedly and used by all members of the group when danger is perceived; (2) ya – excited animals around the alpha, towards alpha and towards perceived danger; (3) eh-eh – threat towards potential danger, but especially adult females; accompanied with open mouth showing teeth (OMT); (4) squeaky hinge – threat given especially by young animals; (5) squeal – conflict within the group during a fight; (6) whistle – conflict in the group of a young animal; (7) ahr – a lost animal; others answer this call, apparently to direct it back to the group; (8) uh!uh!uh! – a common vocalization during feeding which may allow contact to be maintained and show general contentment; (9) uch!uch! – an animal trying to keep up with the group; (10) warble – young animals establishing contact or coming close to an adult; (11) purr – close and pacific contact; (12) chirriar – pacific interaction of young ones during play.

Perhaps the most important display is the behavior of breaking branches, which all members of the group carry out. Even infants break small branches (or twigs), letting them fall to the soil, but the most spectacular is the alpha male who chooses large, dry branches which he hits with his hands and feet in spectacular jumps, so that they fall. Usually such branches make a tremendous sound as they fall through the other branches, and the members of the group become very excited and chatter loudly. This behavior is quite commonly discharged towards an observer when the animals have lost their fear.

Tool use

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Trinidad white-fronted capuchins have been observed using leaves as cups to drink water from tree cavities.[33]The leaves used were modified before by changing the shape of the leaf. The leaves are discarded after one use, meaning that a different leaf is used for repeat visits.[33]These observations suggest that, like thecommon chimpanzee,wild capuchins demonstrate tool manufacture and use in foraging-related contexts.[33]

Interspecific interactions and predators

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White-fronted capuchins frequently travel withsquirrel monkeysand also sometimes travel with thetufted capuchinandVenezuelan red howler.Thedouble-toothed kiteoften accompanies these monkeys, exactly as it does other species of primates. White-fronted capuchins feel threatened by avian predators, and they are very vigilant around any large bird of prey. In Vichada, Colombia,tayra,Boa constrictorand theornate hawk-eaglehave been seen trying to capture white-fronted capuchins.[27][29]After detecting the tayra andBoa constrictorthe members of the troop showed little fear and caution, even though these animals threatened the monkeys. The most common behavior after detecting a potential ground predator is "ya-ya" vocalization and branch breaking over the head of the potential predator, similar to the display of thebrown woolly monkey.In contrast, after being frightened by a male ornate hawk-eagle the monkeys screamed intensely only once, then hid quietly, some descending to the ground to sneak away.[27][29]

Conservation status

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White-fronted capuchins are adaptable and have a wide distribution. Nevertheless, some species are under considerable pressure. TheEcuadorian white-fronted capuchinis listed as "critically endangered" by theIUCN,and thevaried white-fronted capuchinandSanta Marta white-fronted capuchinare listed as "endangered."[38]The IUCN does not have enough data to evaluate theRío Cesar white-fronted capuchin.[38]Also, theshock-headed capuchin,C. cuscinus,is found only is a small part of the SW Colombian Amazon and probably should be classified as "vulnerable" for the country.[39]We need to census the various subspecies and to clarify the taxonomy in order to evaluate properly the situation within the country. White-fronted capuchins are found within 10–15 National Parks and are probably not excessively hunted.[40]Also, they survive well in secondary vegetation close to human beings

References

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Books cited

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