7—
New World Monkeys: Cebids

Scientific Name1

Common Name

AOTINAE

 

Aotus sp.

night monkey, owl monkey, dourocouli

Aotus griseimembra

night monkey, owl monkey

Callicebus sp.

titi monkey

PITHECIINAE

 

Pithecia sp.

saki

Chiropote sp.

bearded saki

Cacajao sp.

uacari

CEBINAE

 

Cebus sp.

capuchin monkey, organ-grinder monkey

Cebus albifrons

brown and white capuchin

Cebus apella

brown or tufted capuchin

Cebus capucinus

white-faced capuchin

Cebus olivaceus

wedge-capped or weeper capuchin

Saimiri sp.

squirrel monkey

Saimiri boliviensis

Roman arch squirrel monkey

1  

This is a list of scientific and common names of species discussed in this chapter, not a comprehensive taxonomic list.



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--> 7— New World Monkeys: Cebids Scientific Name1 Common Name AOTINAE   Aotus sp. night monkey, owl monkey, dourocouli Aotus griseimembra night monkey, owl monkey Callicebus sp. titi monkey PITHECIINAE   Pithecia sp. saki Chiropote sp. bearded saki Cacajao sp. uacari CEBINAE   Cebus sp. capuchin monkey, organ-grinder monkey Cebus albifrons brown and white capuchin Cebus apella brown or tufted capuchin Cebus capucinus white-faced capuchin Cebus olivaceus wedge-capped or weeper capuchin Saimiri sp. squirrel monkey Saimiri boliviensis Roman arch squirrel monkey 1   This is a list of scientific and common names of species discussed in this chapter, not a comprehensive taxonomic list.

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--> Saimiri oerstedii gothic arch squirrel monkey Saimiri sciureus gothic arch squirrel monkey Saimiri ustus gothic arch squirrel monkey ATELINAE   Ateles sp. spider monkey Brachyteles sp. woolly spider monkey Lagothrix sp. woolly monkey ALOUATTINAE   Alouatta sp. howler monkey The family Cebidae includes 11 genera: Alouatta (howler monkeys), Aotus (night or owl monkeys), Ateles (spider monkeys), Brachyteles (woolly spider monkeys), Cacajao (uacaris), Callicebus (titi monkeys), Cebus (capuchin monkeys), Chiropotes (bearded sakis), Lagothrix (woolly monkeys), Pithecia (sakis), and Saimiri (squirrel monkeys). The most comprehensive references available on the natural history of these genera are the two volumes in the series Ecology and Behavior of Neotropical Primates (Coimbra-Filho and Mittermeier 1981; Kinzey 1997; Mittermeier and others 1988). The taxonomy of these genera is still being revised; according to one authoritative source (Mittermeier and others 1988), revisions are likely to increase the number of recognized species and subspecies. The squirrel monkeys are the most common cebids in laboratory environments. Opinions vary about the number of species, and Hershkovitz (1984) has argued for the recognition of four species. On the basis of the pattern created by pigmentation and the white hair around the eyes, squirrel monkeys have been described as gothic arch (Saimiri sciureus, S. oerstedii, and S. ustus) or roman arch (S. boliviensis) (Hershkovitz 1984). Variation in head and body color from yellow-orange to black to gray-green is noted among species and subspecies. Species have pronounced differences in susceptibility to experimentally induced diseases and social behavior. Differences in the number of acrocentric autosomes are noted in karyo-types among species and subspecies of squirrel monkeys. The "squirrel monkey" is clearly several kinds of monkey. Aotus (the night or owl monkey, also sometimes called the dourocouli) is found in many laboratories and should be recognized as a group of nine species (Hershkovitz 1983). Differences in dipliod chromosome numbers among karyo-types exist, and one who ignores these differences cannot readily form breeding pairs. Species of Cebus are often in exhibits and increasingly often in laboratories. Various common names have been applied to these "organ-grinder monkeys." Most are called capuchins with an inconsistent use of modifiers, such as wedge-capped or weeper (C. olivaceus), white-faced (C. capucinus ), and brown and

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--> white or white-fronted (C. albifrons). Cebus apella (the tufted or brown capuchin) is perhaps the most commonly seen. The other genera of Cebidae are less commonly seen in captivity, although woolly monkeys (Lagothrix) enjoyed an unfortunate early popularity in the pet trade, and spider monkeys (Ateles) are often seen in exhibits. Genera in the Cebidae share only a few features of ecology, social organization, and life history. All are primarily arboreal, and all except Aotus are diurnal. The basic locomotor pattern for all genera is quadrupedal walking, but capuchins, howler monkeys, spider monkeys, woolly spider monkeys, and woolly monkeys have prehensile tails, which are used in various degrees to support the body. All those can hang suspended by the tail alone, and the last four are considered "semibrachiators," meaning that they often suspend themselves from supports using only their hands and tail. Most cebids are agile climbers and capable of substantial leaps. With the exception of the uacaris, whose tails are only one-third as long as their bodies, the tail is usually longer than the body in cebids. Spider, woolly, howler, and woolly spider monkeys have a naked "fingertip" at the end of the tail, and they use the tail not only in brachiation but also to manipulate objects not within hand reach. The genera differ markedly in appearance, from the striking bald head and distinctive coat color of the red or white uacaris to the spiky hair of the spider monkey and black uacaris. The adults range in size from Saimiri, at about 750 g (1.6 lb), to the Lagothrix, at nearly 10 kg (22 lb). Cebids generally show far less sexual dimorphism than Old World monkeys, and males are often only slightly larger than females. In contrast with other primate groups, in which sexual dimorphism increases with body size, the largest cebids are relatively monomorphic in size. However, the two sexes in sakis and some species of howler monkeys are of different color, even though of similar size; a naive observer might think that the two sexes were of different species because the color difference appears even in infancy. Life history characteristics also vary among genera (Napier and Napier 1967, 1985). Infants nurse for from as little as 3 or 4 months (Saimiri , Callicebus, Pithecia, and possibly Chiropotes) to 2 years or longer (Ateles and Lagothrix). Average interbirth intervals range from 1 year to 2.5 years (or longer). Maximal life span (in captivity) varies from about 25 years for squirrel monkeys and titis to nearly 50 years for capuchins (and probably spider and woolly monkeys as well). All genera except Callicebus, Pithecia, and Aotus (which are monogamous) live in mixed-sex groups; modal group size and organization vary widely among species. Diets also vary widely; some species are nearly completely folivorous (eating a diet of leaves), some are frugivores, and some are omnivores. Many species are found in association with other primate genera whose ecological niches overlap; this is especially common for Saimiri with Cebus apella. Differences among genera in ecology and behavior are enormous, as should be expected by the length of evolutionary time that they have been radiating into

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--> specialized niches in their natural environment. Moreover, their ecology and behavior are quite divergent from those of Old World monkeys, in line with the differences in habitat types and predator and competitor complements. The net result of their history of adaptive radiation in a particular setting is that virtually all aspects of captive management of these species should be tailored to the individual species to accommodate the variations among them in size, diet, social organization, reproductive cycles, locomotor patterns, and activity levels. In the remainder of this chapter, general points are presented where possible, and specific recommendations relevant to husbandry and well-being for particular genera that differ from these general points are noted. Housing The vertical dimension appears to be more important for these nonhuman primates' use of space than the horizontal dimension. Housing should provide adequate vertical space and postural supports to enable all animals to move and perch with their tail hanging in a normal position of rest without touching the floor. Perches with multiple heights within the enclosure are desirable. Space should permit jumping laterally and vertically. Climbing structures, swings, and other flexible supports are used by animals of all ages in some species but especially by youngsters. The ground or floor is used by some species if low perches or objects on the floor make vertical movement easy and if the floor is a "soft" material (such as a covering of straw or wood chips). Bedding material supports species-normal exploratory activity in capuchins and other manipulative species; supports foraging activities if small food items, such as sunflower seeds, are scattered; and reduces the likelihood of injury or hypothermia in infants that fall to the floor. Cage furnishings should also permit the use of the tail and suspensory postures in genera with prehensile tails, e.g., spider monkeys. Large cebids do well at normal to high temperatures of 21–29°C (70–84°F); however, smaller cebids such as squirrel monkeys seem to do better at temperatures in the higher end of this range (e.g., 26–29°C, or 78–84°F). If outdoor housing is used, warming areas are needed for most species if the ambient temperature falls below 10–15°C (50–59°F). It should not be assumed that animals will spontaneously seek out the sheltered areas when the temperature falls. Titi monkeys, for example, will remain in a preferred outside sitting spot, and spider monkeys will sunbathe even when temperatures are dangerously low. Animals might need to be confined in heated quarters under such conditions. Cebids eat small amounts of food over long periods of each day. They often nibble a bit of food and then drop it, perhaps to retrieve it again later. Food presented in a pan is usually removed by the animals as soon as it is delivered. In enclosures with raised mesh floors, food often drops below the mesh floor, and special efforts are required to ensure that food is available ad libitum. The owl monkey (aotus) should be provided with a nest box. A reversed

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--> light cycle is recommended with caregivers active during the "night" phase, when the area can be illuminated by red light. Because cebids lack ischial callosities for sitting, they must "perch" using their feet rather than sit. Squirrel monkeys are likely to develop pressure sores on the dorsal surface at the base of the tail unless they are provided suitable perches and climbing structures, so it is important that appropriate materials be selected for the construction of perches (Abee 1985). Furthermore, pressure sores can occur in weakened animals that are unable to assume a proper perching posture. Squirrel monkeys are prone to hypothermia, especially if they are stressed, and materials that are poor thermal conductors or thermoneutral (such as wood and PVC pipe) are preferred over metal, particularly in environments in which the ambient temperature can fall below 24°C (75°F) (Abee 1989). At lower temperatures, the animals assume a "huddle" posture in which the back is arched and the tail is wrapped around the body. The same posture can be seen when the animals are sleeping, resting, or ill. At higher temperatures, squirrel monkeys "sprawl'' by straddling a perch or branch and allowing the limbs and tail to hang below. Squirrel monkey housing should be designed so that animals do not need to walk on wet abrasive floors, because animals are prone to develop contact dermatitis if forced to spend long periods in direct contact with urine-soaked concrete surfaces. Nutrition Most cebids maintain good health when fed commercial monkey chow that is specifically formulated for New World monkeys (i.e., is rated as high in protein—at least 25%—and contains vitamin D3) supplemented daily with fresh fruits and a vitamin-mineral supplement. Diets containing less protein and fat and more fiber might be preferable for some genera, such as Aotus, which have large ceca adapted for digestion of fruits and leaves. Furthermore, species prone to renal disease might benefit from reduced-protein diets. Vitamin supplements can be supplied by mixing them with fruit pieces or with a soft food base (such as yogurt, applesauce, infant cereal, or cooked grains). Some species (squirrel monkeys and capuchin monkeys) appear to need more folic acid than what is provided in commercial chow, particularly to support pregnancy and growth (Knapka and others 1995; Rasmussen and others 1982); consideration should be given to folic acid supplementation as necessary. Howler monkeys are the most folivorous of the New World monkeys and are nutritionally difficult to maintain in captivity (Benton 1976; Shoemaker 1979, 1982). Strong tea instead of water has been suggested to provide the tannins that they normally obtain from leaves. Large amounts of leafy greens supplemented with Lactobacillus acidophilus are also recommended. Aotus does well when given commercial diets with 5% or less fat and a high fiber content. Some taxa (such as A. griseimembra) might require supplemental

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--> parenteral administration of alpha-tocopherol (vitamin E) to prevent vitamin E-responsive anemia lest clinical signs, including severe anemia and myopathy, develop. This can occur in animals whose baseline serum vitamin E levels appear normal (Meydani and others 1983; Sehgal and others 1980). Social Behavior Members of monogamous genera (Aotus, Callicebus, and Pithecia) have been successfully housed in captivity as mated pairs with offspring. Introducing adult strangers of the same sex is not always possible. Adult male night monkeys are aggressive toward one another; females can be housed together, but newly formed pairs should be observed to confirm compatibility. It is not known whether this applies to the other monogamous genera. In monogamous species, it is sometimes possible to maintain offspring in the natal group until they reach sexual maturity. In cebids of polygamous genera, group size in captivity is limited mainly by space. Capuchins and squirrel monkeys have been maintained in groups containing 35 members or more with multiple adult males present. The introduction of new members to a group is usually problematic, especially if adults of the same sex are already resident. Considerable variation is to be expected. Given adequate space, woolly and spider monkeys can be kept in groups with multiple adult males. Adult male squirrel monkeys generally tolerate each other well in the absence of adult females, but fighting can occur if mixed-sex groups are formed at the start of the breeding season. Many cebids readily accept an animal returned to the group after a week or more, and capuchins can be safely returned even after several months. Any major social reorganization that occurs in the absence of an individual animal complicates its return. Return of animals to large social groups appears to be easier if it occurs with only a portion of the home group present and if the small group is allowed to return to the main group a few minutes later. Spider monkeys are particularly excited by reintroductions, and such events warrant careful monitoring. Attacks on infants occur occasionally in capuchins and in woolly, howler, and spider monkeys. The precursors of attacks are generally not evident, and animals behave tolerantly with infants under normal circumstances. It is thought that social instability can trigger attacks on infants. As with the callitrichids, many cebids form polyspecific associations in the wild and are quite tolerant of extraspecifics. Squirrel monkey and capuchin associations are particularly common in the wild, but squirrel monkeys carry Herpes tamarinus and should be kept isolated from night monkeys and susceptible callitrichid species (Adams and others 1995). Mixed-species assemblages have otherwise been maintained in exhibits without adverse consequences. Cebids use feces, urine, genital discharge, saliva, and secretions from specialized scent glands in the skin for the purpose of scentmarking. Sniffing and

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--> licking urine, scent marks, or the bodies of conspecifics are common in all species. Techniques vary, but urine washing and distribution of urine over parts of the body occur in various forms in most genera. Titi, woolly, and spider monkeys distribute saliva over parts of the body, including a sternal gland on the chest. Capuchins and uacaris rub plants and other items in their environment into their fur. Chemical signals might identify an individual animal's sex and play important roles in reproductive behavior, aggressive interactions, and other kinds of behaviors. Sanitation procedures should take into consideration the possible importance of odors for the cage inhabitants. The presence of odors in a monkey run should not be taken to mean that sanitation is inadequate (Williams and Bernstein 1995; see also "Sanitation" in Chapter 3). Reproduction and Development Age at reproductive maturity ranges from 2 years in Saimiri, Callicebus, and Pithecia to 5–6 years in Lagothrix, Ateles, and Cebus. Members of some genera breed seasonally (e.g., Saimiri and Cacajao); members of others (such as Cebus) do not. In some genera, females exhibit marked proceptive behavior (i.e., they seek out and actively solicit a male) and mate preferences. Duration of gestation in cebids ranges from about 4.5 months (in Aotus) to 7.5 months (in Ateles) (Napier and Napier 1985). Single births predominate. Infants can cling unaided from birth but do not locomote independently for several weeks to several months; they ride dorsally soon after birth (the precise age at which dorsal riding begins varies with the genus, from birth to about 2 months). However, in some genera (capuchins, woolly monkeys, and spider monkeys), mothers often cradle infants ventrally for extended periods and assist a newborn infant in clinging to the ventrum if the mother moves while it is in a ventral position. In the monogamous genera (night monkeys and titis; there is no information on this point for sakis), infants are routinely carried by fathers when they are not nursing. In capuchins and squirrel monkeys, infants can be carried by adults and juveniles other than the mother (Fragaszy and others 1991; Williams and others 1994). The period of infant dependence varies among genera; in the larger forms (e.g., Ateles), infants can remain on the mother and nurse for up to 2 years. Nursing periods among cebids are generally longer than is typical of Old World monkeys. In species in which both parents are involved in infant care (titi, night, and owl monkeys), rejection of an infant by either parent might require human intervention. A male titi can provide adequate care for an infant rejected by its mother, but the infant will require hand feeding. Male titis can be box-trained and exhibit little protest when an infant is gently removed, fed, and returned. When a father rejects an infant, the mother alone often becomes agitated with the

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--> constant burden of the infant. If such signs occur, the infant might have to be removed to prevent injury. Male squirrel monkeys display an unusual pattern of seasonal "fatting." Males can gain 20–30% in body weight and become noticeably bulkier in the shoulders and upper torso as the breeding season approaches. Not all males show this change—it is most commonly observed in the Roman Arch species—and it is not required for fertility. Males gradually lose the weight during the course of the breeding season. Cognition Cognition in squirrel monkeys, capuchins, and some of the other New World and Old World genera has been reviewed by Rumbaugh (1967) and Fragaszy (1985). Cebids seem generally similar to rhesus monkeys in several cognitive capacities, although they appear to be somewhat less able in conceptual and relational learning tasks. There is, however, wide latitude in their activity levels and responsiveness to the physical and social environment. Capuchins, for example, show greater manipulative ability than rhesus monkeys and are the prototype of the active monkey for which provision of opportunities for productive activity is essential to well-being. When not locomoting, they are most often busy with their hands (Fragaszy and Adams-Curtis 1991). When no other opportunities are present, their attention is directed to surfaces in the cage or nearby objects, such as locks. This activity can be safely redirected by providing them with such objects and materials as wood, soft plastic, straw, and small containers (Fragaszy and Westergaard 1985; Visalberghi 1988). They will spend much time shredding and destroying disposable objects. They also retain interest in objects that require dexterous probing or scraping (Fragaszy and Visalberghi 1989; Westergaard and Fragaszy 1987; Westergaard and Suomi 1993). Other cebids are less manipulative than capuchins; Aotus and Callicebus perhaps are least so. Monitoring other members of the social group appears to be more important to these animals than physically interacting with the inanimate environment. Personnel New World monkeys (cebids and callitrichids) in general are less likely to be aggressive toward humans than the more common species of Old World monkeys. They often exhibit curiosity toward humans and do not respond aggressively when prolonged direct eye contact is made. They will often approach familiar people and readily accept food or objects offered by hand. That can be useful when supplementing the diet or medication of particular animals (Abee 1985). It might be necessary to get a timid animal away from other group members for such supplementation.

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--> Despite their generally unaggressive behavior toward humans, New World monkeys will resist restraint and can deliver serious bites in self-defense. An animal attempting to climb on and explore a human might bite vigorously if pushed away or frightened. Former pet animals are especially likely to cause problems. They can form strong attachments to some people and "defend" favored people against other people. Personnel should avoid sudden movement and loud noises in animal areas; this might be especially important when they are dealing with night monkeys, titis, and especially newly arrived woolly monkeys. Night monkeys seem particularly sensitive to loud noises and changes in routine. Titis might "freeze" and exhibit labored breathing in unfamiliar environments and exhibit similar signs of distress when confronted with changes in their environment. Woolly monkeys sometimes become lethargic and refuse to eat on first arrival at a facility. Extensive gentle attention from a well-trained person is often effective in helping these animals to adjust to a new environment. Most cebids quickly learn to recognize familiar people and will respond to them in accord with the nature of their experiences. Technicians who deal with the daily care of these animals should interact with their charges primarily in ways that are pleasant for the animals. If they can avoid it, they should not participate in capture or restraint procedures. When it is necessary that such personnel participate in activities that the animals find aversive, the use of a distinctive uniform only for such occasions might facilitate the re-establishment of good relations during routine husbandry. Personnel should routinely devote some time to positive interactions with animals, such as provision of vegetables and fruit rewards during daily observation. Most cebids will readily move from one cage to another for cleaning and maintenance tasks, and every effort should be made to avoid wetting the animals or requiring them to move across wet floors. They can also be trained to enter transport boxes for individual handling, and this obviates capture with gloves or nets. Veterinary Care The veterinary medical care of cebids is similar to that of callitrichids, and readers are referred to the "Veterinary Care" section of Chapter 6 also. In addition to attention to the nutritional requirements of cebids, veterinary personnel should be vigilant for signs of dehydration. Relatively small primates, such as squirrel monkeys, can dehydrate quickly. Squirrel monkeys can dehydrate and develop hypoglycemia in less than 24 hours if their access to water is disrupted (Abee 1985). They will not feed without water, and many New World monkeys will show adverse effects if deprived of food for a day. Most eat more or less continuously during the daylight hours. Stress responses, mentioned previously, can also influence feeding and drink-

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--> ing. Juvenile squirrel monkeys stress easily and can become dehydrated as a consequence. Spider and woolly monkeys seem particularly susceptible to stress associated with restraint and handling. Woolly monkeys also seem to show a high frequency of high blood pressure, and veterinary procedures should take this into account. Cebids are susceptible to most of the common viral upper respiratory illnesses that people develop (Adams and others 1995). Personnel who have symptoms of such illnesses should avoid working closely with animals. Measles is also readily transmitted to New World monkeys. Night monkeys are particularly susceptible to viral diseases of humans, such as Herpesvirus simplex and measles (Weller 1994). Personnel should not be allowed to work with night monkeys if they have cold sores. Personnel that have family members with measles should not work with cebids. Personnel who have been vaccinated against measles should not have contact with cebids for at least 2 weeks after vaccination. Several diseases that occur commonly in night monkeys are uncommon in other neotropical primates. Dilative and hypertrophic cardiomyopathy, possibly the result of chronic hypertension, is peculiar to night monkeys and can lead to sudden death or chronic heart failure (Weller 1994). Chronic glomerulonephritis is commonly observed in aged animals (Abee 1985; Chapman and others 1973; Hunt and others 1976; Stills and Bullock 1981). Hemolytic and necrotizing myopathy responsive to vitamin E supplementation has been observed in Aotus griseimembra (Weller 1994). Medical management of the diseases of night monkeys is complex and requires close veterinary supervision. Cebids are susceptible to a number of intestinal parasites, but the usual veterinary medical treatment for such problems is generally effective. A well-planned program of examinations and treatment will prevent most disease problems. Cebids appear to be more resistant to tuberculosis than are Old World monkeys; few problems with this disease have ever been reported. But Herpes tamarinus, which can cause serious disease in callitrichids, is also a serious problem for night monkeys and is often carried by squirrel monkeys without producing clinical signs (Adams and others 1995). As a general policy, squirrel monkeys should be housed in isolation from night monkeys and from susceptible callitrichid species. (Consult Appendix B for a list of diseases known to be transmitted among primate taxa.) One other problem that the veterinary staff should be alert for is the possible development of gestational diabetes in woolly monkeys. Captive management of New World monkeys remains relatively poorly understood, and vigilance on the part of the veterinary and husbandry staff is the best precaution possible. Cebids are not known to pose any special bacterial- or viral-disease hazards to the humans that interact with them. Therefore, personnel bitten or scratched by a New World monkey can be treated in a similar way as bites and scratches from a dog or cat (NRC 1997a).