Sapajus apella (Linnaeus, 1758)
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publication ID |
https://doi.org/ 10.5281/zenodo.6628559 |
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DOI |
https://doi.org/10.5281/zenodo.6628253 |
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persistent identifier |
https://treatment.plazi.org/id/560F8786-B729-285A-08EC-F572384FFC83 |
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Jonas |
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scientific name |
Sapajus apella |
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Guianan Brown Capuchin
French: Sapajou brun / German: Haubenkapuzineraffe / Spanish: Capuchino pardo
Other common names: Black-capped Capuchin, Brown Capuchin; Margarita Island Capuchin (margaritae)
Taxonomy. Simia apella Linnaeus, 1758 ,
“America.” Restricted by E. Geoffroy Saint-Hilaire in 1812 to “Cayenne, French Guiana.”
Taxonomy of Amazonian robust/ tufted capuchins is still not well understood. Eight Amazonian subspecies of Cebus apella were listed by W. C. O. Hill in 1960. These were largely ignored because of their uncertain distributions and difficulties of understanding regional variation or patterns, with so much variation in tufts and color patterns. C. P. Groves in 2001 listed five of Hill's subspecies as valid species or subspecies. J. S. Silva,Jr. in 2001 argued for the existence ofjust two Amazonian robust capuchin species: S. apella in the eastern and central Amazon Basin and S. macrocephalus (recognized as a subspecies of apella by Hill) in the western Amazon Basin. Following Silva, S. apella includes, as a junior synonym, C. fatuellus tocantinus, named by Lonnberg in 1939—a dark capuchin from Cameta, Rio Tocantins, Brazil (recognized by Hill and Groves). Preliminary genetic studies byJ. W. Lynch Alfaro and her coworkers indicated that apella and macrocephalus may not be distinct taxa, but further studies are needed. Two subspecies recognized.
Subspecies and Distribution.
S. a. margaritae Hollister, 1914 — highlands of E Margarita I, Venezuela (Serrania de El Copey and the Cerros El Tamoco, Tragaplata, La Yalla, and Matasiete). View Figure
Descriptive notes. Head-body 38-46 cm,tail 38-49 cm; weight 2-3—4-8 kg (males) and 1.3-3.4 kg (females). The Guianan Brown Capuchin is large and somewhat heavily built, with a broad head, flat face, and short limbs. The coatis long and coarse, with extremities noticeably darker than the rest of the body. It is generally gray-fawn to dark brown above, with a yellowish or red underside. Lower limbs and tail are black, and there is a variably well-developed dorsal stripe. The face is light gray-brown, and the characteristic crown tuft consists of a thick mat of erect black hairs, forming short tufts above the ears. This gives the top of the head a flat, squared-off or “eared” frontal outline or, alternately, elongated at each frontalside to form “horns.” The black crown of the Guianan Brown Capuchin forms a slight vertex on the forehead (not extending to the nose), and there is whitish line framing the face, forming a slight arch above the eyes. The face and temples are light gray-brown. The darker area above the eyes gives the appearance of eyebrows. The crown cap extends down the cheeks as a distinct, thick black bar in front of each ear; these “sideburns” often meet below the chin. Sexes are similar, but males are a bit heavier and often considerably darker. The “Margarita Island Capuchin” (S. a. margaritae) is darker than forms from the upper Orinoco in Venezuela. Dark sideburns in front of the ears are longer (extending from crown to throat) and more defined than in the nominate subspecies of the Guianan Brown Capuchin. When tufts are present, they are longer in the nominate form than in the Margarita Island Capuchin. In the Margarita Island Capuchin, outsides of upper arms and shoulders are a pale-yellow straw color. Wrists, ankles, and inner forearms are black, thighs and rump are brindled (pale yellow) brown, and flanks, lower back, and upper chest are pale brown, becoming paler on the upper back to the neck. There is a dark midline stripe down the back. The face is grayish, tinged pink on the cheeks and chin, with sparse whitish hairs on the temples and around the mouth. The face is framed by a black line extending from the black cap to sideburns to the throat. The black cap extends in a “V” to between the eyes, with small round tufts above each eye. The form from the Rio Tocantins Basin is dark gray-fawn to dark chestnut-brown, with reddish undersides and flanks. There is a trace of a dorsal stripe. Forearms, thighs, shanks, feet, and tail are black. The head is also black with little trace of white, and crown tufts are well developed.
Habitat. A wide range of forest types: lowland, submontane (700-1000 m above sea level), and montane forests of the Guiana and Brazilian shields of the central and eastern Amazon Basin, including seasonally inundated forests, tidal flooded forest (tidal varzea) in the delta region of the Amazon River, mangrove forest and palm swamp forest, liana forest (“mata de cip6”), gallery forest and forest patches in the Roraima and Amapa states savannas, and open-canopied babassu palm (Orbignya) forest on the south-eastern border of the Amazon River in the states of Maranhao, Goias, and Para. Although the geographic distribution of the Guianan Brown Capuchin includes sclerophytic, small-leaved, white-sand forests (“caatinga alta” or “campinarana,” also Wallaba forest in the Guianas) and scrub (“caatinga baixa” or “campina”) typical of the Rio Negro Basin and also Serra do Cachimbo on the Para State/Mato Grosso State border, it is not known to what extent they occupy them. The Margarita Island Capuchin is confined to isolated montane forest patches in the eastern part of the island, including pre-montane dry forest, humid montane and pre-montane forest, and disturbed (broken canopy) palm forest (“cocal”).
Food and Feeding. Diet of Guianan Brown Capuchins consist of fruits and seeds (68%), small animal prey (197%), and other items such as palm heart, the rachis of palm leaves, and the succulent bases of bromeliad leaves (12:3%). In a study by W. Spironello near Manaus in the Central Amazon, six species of palms ( Arecaceae ) figured prominently in the diet of a group of 9-14 Guianan Brown Capuchins, particularly two species: Jessenia (= Oenocarpus ) bataua and Maximiliana (= Attalea ) maripa. They ate the albumen (endocarp) of immature fruits and the mesocarp of mature fruits of these two species and Oenocarpus bacaba, Astrocaryum munbaca, Mauritia flexuosa, and Syagrus inajai. In the early dry season, 42% of all records of fruit feeding were of palms fruits, peaking at ¢.52% in July. Throughout the year, the group ate fruits, seeds, nectar, gum, inflorescences, pith, and petioles from more than 200 plant species. Besides palms, the other plant families most commonly found in the diet included Sapotaceae ( Micropholis , Chrysophyllum , Pouteria ), Moraceae ( Brosimum , Ficus ), Urticaceae (Pourouma) , Fabaceae (Inga) , Euphorbiaceae (Micrandropsis) , Goupiaceae (Goupra glabra), and Lecythidaceae . This group of Guianan Brown Capuchins had a very large home range of ¢.850 ha, probably because of the low density of palms in the area. Further north in Suriname and Guiana, where rains are also very seasonal, palms Socratea exorrhiza and Maximiliana maripa are important to Guianan Brown Capuchin in the dry season. In Suriname, the Guianan Brown Capuchin’s propensity to pound hard fruits is particularly applied to the thick-husked woodyfruits of the Brazil nut family, Lecythidaceae . When immature, the fruit is relatively soft, and the reward of seeds rich in lipids, proteins, and carbohydrates easily compensates for difficulties of getting at them. In a study at the Nouragues Field Station, French Guiana, S. Zhang found that Guianan Brown Capuchins ate mostly fruits during the wet season (December— June), peaking in March—June when 80-99% of the diet was fruit. In the dry season (October), fruits comprised as little as 30% of the diet, which was supplemented by flowers, pith, stems, petioles, and leaves and an increase in the time spent foraging for animal prey. Guianan Brown Capuchins eat freshwater crabs ( Pseudothelphusidae ) along river banks. They eat oysters (Crassostrea rhizophorae) from mangrove swamps, banging them with oyster shells until they weaken and open. Vertebrate prey includes frogs, lizards, birds, and small mammals such as mouse opossums (Marmosa). The diet of the Margarita Island Capuchin, studied by L.. Marques and V. Sanz in 1989-1990, was 50-9% fruits, 24-6% insects, 14% pith, 3:5% petioles, 3-5% seeds, and 3-5% flowers. Animal prey include Hymenoptera (ants: adults, larvae and pupae), Orthoptera, and Coleoptera. Guianan Brown Capuchins use similar methods to forage for animal prey and exploit palm fruits as do Large-headed Capuchins (S. macrocephalus ).
Breeding. The menstrual cycle of the Guianan Brown Capuchin is 20-8 days; menstruation lasts three days, sometimes evidenced by a minimal menstrual bleeding. Births peak in October—January. Normally only one offspring is born at a time. Mean interbirth interval in captivity is 20-6 months (n = 23 successive births). Males are directly involved with the young or are at least tolerant of them. Females are fully adult at c.4-5 years, but males take longer to mature (up to eight years in some cases). As in other species of Sapajus , females show proceptive behavior during the periovulatory period, ending on the sixth day when ovulation occurs. The female stays with the alpha male, showing courtship behavior: grimacing, eyebrow raising, circling the male, presenting and touching him, and making mating calls. The male is slow to respond but eventually may mount several times. This courting can continue for up to four days; on the fifth day, the alpha male follows the female and interferes with subordinate males attempting to mate with her. On the sixth day, the alpha male leaves the female. She may then mate with subordinate males, but without prolonged courtship, and the partners separate immediately after mating. Gestation is c.155 days. Neonates weigh ¢.210 g (range 170-260 g), or ¢.9% of the mother’s weight. Neonatal growth is rapid for eight weeks after birth but then slows. Female Guianan Brown Capuchins stop growing at aboutfive years old, but males continue to gain weight for another couple of years. In captivity, males are fertile when they are a little more than four years old, but in the wild, they probably do not breed for another few years when they can secure a position as an alpha male. Females are fertile and able to reproduce atfive years old.
Activity patterns. In a study in the Nouragues Field Station, activity patterns varied during the year, influenced largely by food availability and dispersion. In the wet season when fruits were abundant and widespread, Guianan Brown Capuchins tended to travel more widely. Throughout the year, feeding on fruits took up 20-30% of the day, foraging for animal prey 20-35%, travel 20-30% (more time was spent in travel in December—January in the early wet season), 5-10% resting, and 4-15% in other activities (e.g. grooming and play). When traveling and foraging, they generally used middle and lower canopies and understory, 10-20 m above the ground. Sleeping sites in the Manaus and Nouragues studies were typically in crowns oftall (20-25 m) Jessenia palms, where individuals could lie flat on the leaf bases and where access to the tree was limited to fronds, providing some protection from mammalian predators.
Movements, Home range and Social organization. The Guianan Brown Capuchin lives in single-male or age-graded (with a single dominant male) groups of generally 10-20 individuals, including up to five adult females. The Margarita Island Capuchin lives in small single-male groups of 4-6 individuals, including 1-2 adult females, subadults, and juveniles. The geographic distribution of the Guiana Brown Capuchin largely coincides with the Guiana and Brazilian shields, very ancient rock formations with nutrient poor soils compared with alluvial plains of the western Amazon Basin, occupied by the Large-headed Capuchin. Forest productivity of the shields is low, and home ranges tend to be large, from 355 ha at the Nouragues Field Station in French Guiana to 850 ha north of Manaus. At Manaus, daily home ranges were 34-70 ha and daily movements were 2236-4560 m. In this terra firma forest, Guianan Brown Capuchins spent 39% of their time in areas of poorly drained soils along streams where their favored palm, Jessenia bataua, was found. They typically slept in these palms (92% of the recorded sleeping sites). Daily movements were longer in the wet season when fruit sources were more widespread. A similar pattern was found in Nouragues where daily movements were 1746-3469 m (average 2268 m) and were longer in December—January when fruiting trees were neither scarce nor abundant but widespread. Small groups of Margarita Island Capuchins occupy home ranges of ¢.30 ha. Predators include forest cats and the large raptors.
Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as Cebus apella ), with the Margarita Island Capuchin classified as Critically Endangered (as C. a. margaritae). The Guianan Brown Capuchin is intensively hunted for meat, particularly where the larger atelines have already been hunted out. It is adaptable, however, and wide ranging in the remotest and most untouched areas of the Amazon Basin to the north of the Amazon River. To the south of the river, enormous areas of forest are being destroyed in northern Mato Grosso and southern Para states in the Madeira and Tapajos basins. The Guianan Brown Capuchin occurs in numerous and large protected areas. The Margarita Island Capuchin is well separated from other robust/tufted capuchin monkeys—the nearest population is in the southern extreme of the Orinoco Delta, ¢.1200 km away—and suffers from a tiny distribution, habitat degradation, illegal hunting, and commerce. Capuchins raid crops and are considered to be pests and persecuted, even though they are also favored as pets. Possibly a further threat to the Margarita Island Capuchin is the recent introduction of the Guianan Weeper Capuchin ( Cebus olivaceus ) to Margarita Island, where they may compete for diminishing habitat. The Margarita Island Capuchin occurs in Cerro El Copey National Park (7130 ha), but parts of the Park are being encroached upon and there is illegal logging. It is also found in Cerro Matasiete y Guayamuri Natural Monument (1672 ha), which affords it some protection.
Bibliography. Boher-Bentti & Cordero-Rodriguez (2000), Boinski et al. (2001), Fernandes (1991), Fernandes et al. (1995), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Guillotin et al. (1994), Groves (2001), Husson (1957), Linares (1998), Lonnberg (1939), Lynch Alfaro, Boubli et al. (2012), Marquez & Sanz (1991), Martinez et al. (2000), Mittermeier & van Roosmalen (1981), Nagle & Denari (1982), Phillips et al. (1994), Port-Carvalho et al. (2004), Rettig (1978), Rylands et al. (2005), Sanz & Marquez (1994), Simmen & Sabatier (1996), Spironello (1991, 2001), Torres (1988), Zhang Shuyi (1995a, 1995b), Zhang Shuyi & Wang Lixin (1995).
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