> Enrichment for Nonhuman Primates
>
> Contents:
>
> **Introduction Page 3**
>
> **Baboons Page 5**
>
> Background (5)
>
> Social World (6)
>
> Physical World (6)
>
> Special Cases (7)
>
> Problem Behaviors (8)
>
> Safety Issues (8)
>
> References (9)
>
> Common Names (10)
>
> **Capuchins Page 11**
>
> Background (11)
>
> Social World (12)
>
> Physical World (13)
>
> Special Cases (14)
>
> Problem Behaviors (14)
>
> Safety Issues (15)
>
> Resources (15)
>
> Common Names (16)
>
> **Chimpanzees Page 17**
>
> Background (17)
>
> Social World (18)
>
> Physical World (19)
>
> Special Cases (21)
>
> Problem Behaviors (22)
>
> Safety Issues (22)
>
> Resources (24)
>
> Common Names (25)
>
> **Macaques Page 26**
>
> Background (26)
>
> Social World (27)
>
> Physical World (28)
>
> Special Cases (29)
>
> Problem Behaviors (30)
>
> Safety Issues (30)
>
> Resources (31)
>
> Common Names (32)
>
> Sample Pair Housing SOP (33)
>
> **Marmosets and Tamarins Page 34**
>
> Background (34)
>
> Social World (35)
>
> Physical World (36)
>
> Special Cases (37)
>
> Safety Issues (38)
>
> References (39)
>
> Common Names (41)
>
> **Squirrel Monkeys Page 44**
>
> Background (44)
>
> Social World (45)
>
> Physical World (46)
>
> Special Cases (48)
>
> Problem Behaviors (49)
>
> Safety Issues (49)
>
> References (50)
>
> Common Names (51)
>
> This series of booklets on enrichment for nonhuman primates\
> was made possible through the cooperation of:
>
> Department of Health and Human Services
>
> NIH, Office of Laboratory Animal Welfare (OLAW)
>
> US Department of Agriculture, Animal Care
>
> Association of Primate Veterinarians
>
> American Society of Primatologists
>
> NIH Publication Numbers:

05-5745 *Baboons*

05-5746 *Capuchins*

05-5748 *Chimpanzees*

05-5744 *Macaques*

05-5747 *Marmosets and Tamarins*

05-5749 *Squirrel Monkeys*

> For more information, contact OLAW at NIH\
> tel: (301) 496-7163, e-mail olaw@od.nih.gov
>
> Introduction
>
> Nonhuman primates maintained in captivity have a valuable role in
> education and research. They are also occasionally used in
> entertainment. The scope of these activities can range from large,
> accredited zoos to small "roadside" exhibits; from national primate
> research centers to small academic institutions with only a few
> monkeys; and from movie sets to street performers. Attached to these
> uses of primates comes an ethical responsibility to provide the
> animals with an environment that promotes their physical and
> behavioral health and well-being. Thus, an obligation is entailed that
> those individuals/institutions caring for captive primates should make
> every effort to ensure adequate veterinary care and husbandry are
> provided, that the animals are housed in appropriate facilities, and
> that as broad a range of species-typical behaviors are able to be
> expressed by the animals as is possible for the captive environment.
>
> This book serves as an introduction to the basic behavior and
> environmental enrichment of several species of nonhuman primates that
> are more commonly used in education, research and entertainment. In
> many ways, this book is meant to be a "how to" manual; it is not
> intended to be a broad scientific review of the primate behavior and
> enrichment literature. The fundamental premise taken throughout each
> chapter is that for an enrichment program to be effective, there must
> be a basic understanding of the biology and behavior of the primate
> species. The species addressed in this series are: baboons, capuchins,
> chimpanzees, macaques, marmosets and tamarins, and squirrel monkeys.
> Each species-section can be read as a stand-alone document without
> need to reference the other sections. This then allows the user to
> distribute the different sections to personnel caring for the specific
> animals.
>
> Each section is divided into five parts: 1) Background, comprised of
> the habitat of the primate, the physical features of the primate, its
> psychological and/or social behavior, and its mating and reproductive
> behavior; 2) Social World; 3) Physical World; 4) Special Cases,
> describing any age-related considerations and concerns associated with
> individual housing; and 5) Problem Behaviors. The content of this
> series has been provided by members of the Association of Primate
> Veterinarians (APV) and the American Society of Primatologists (ASP)
> who have special expertise in the species addressed. This book is
> intended to be a primer because it is, indeed, an introduction to the
> subject of environmental enrichment for primates housed in a diversity
> of conditions. A list of references and/or other resources
> (principally on-line) is provided at the end of each chapter that
> provide additional guidance. The use of scientific references has been
> limited, but should the reader desire more information about a
> specific subject, the links at the end of the sections will provide
> direction to obtaining additional detailed information. Readers are
> also directed to the National Research Council publication, the Guide
> for the Care and Use of Laboratory Animals (1996) and the U.S.
> Department of Agriculture's (USDA) Animal Welfare Regulations to
> review the regulatory requirements of the Public Health Service and
> the USDA for the provision of environmental enrichment.
>
> The APV and ASP wish to thank the Office of Laboratory Animal Welfare,
> in particular Ms. Carol Wigglesworth and Dr. Axel Wolff; the U.S.
> Department of Agriculture/Animal Care, in particular Dr. Chester
> Gipson; and Ms. Dale Feurer, editor, and Ms. Lori Wieder, graphics and
> layout production, for their assistance with this project. The authors
> acknowledge the helpful contributions of Dr. David J. Shepherdson,
> Conservation Program Scientist, Metro Washington Park Zoo; Ms. April
> D. Truitt, Director, Primate Rescue Center, Inc.; and Ms. Kathleen
> Conlee, Program Officer, Humane Society of the United States. Special
> thanks also go to the chapter authors Dr. Christian Abee, Dr. Kate
> Baker, Dr. Linda Brent, Dr. Thomas Butler, Dr. Jeffrey Fite, Dr.
> Dorothy Fragazy, Dr. Jeffrey French and Dr. A. Michele Schuler, and to
> the reviewers from the American Society of Primatologists and the
> Association of Primate Veterinarians.
>
> ---Kathryn Bayne, M.S., Ph.D., D.V.M., DACLAM, CAAB
>
> Editor, Working Group
>
> *This project is dedicated to the memory of Dr. Sylvia Taylor,
> Veterinary Medical Officer, Animal Care, U.S. Department of
> Agriculture, who was a proponent of providing enrichment to nonhuman
> primates and was generous in sharing her knowledge and expertise in
> this regard.*
>
> Baboons
>
> Background
>
> **Habitat**
>
> Baboons live in many parts of Africa, primarily in dry savannah
> woodlands. They are the largest and most terrestrial, or ground
> dwelling, of the cheek pouch monkeys (Cercopithecines). There are five
> types of baboons\--olive, yellow, red, chacma and hamadryas\--which
> may interbreed to form hybrids in captivity and, in some places, in
> the wild. Olive and Yellow baboons are found in many areas of
> equatorial Africa and are typically called savannah baboons. Hamadryas
> baboons inhabit the highlands of Ethiopia. Red or guinea baboons live
> in gallery forest and woodland savannas of West Africa. Chacma baboons
> reside in southern African woodland to semi-desert habitats. Home
> ranges of baboons may cover approximately 10,000 acres.
>
> **Physical Features**
>
> Baboons walk on all four limbs, and their forelimbs and hindlimbs are
> approximately the same size. Males (44 to 53 lbs.) are much larger
> than females (26 to 35 lbs.) and have long canine teeth. The tail is
> moderately long and is typically held in a characteristic U-shape.
> Baboons have prominent ischial callosities, which are bright red in
> some species. They have a prominent muzzle. The life span of a baboon
> ranges from 20 to 30 years.
>
> **Behavior**
>
> Baboons have a number of distinct vocalizations, including:

-   Alarm bark -- loud, rapid, sound to indicate potential threat or
    challenge

-   Lipsmack -- short, repeated clicking of the lips or tongue,
    associated with friendly behavior and approaches to a dominant
    individual or infant

-   Grunt -- low, snort-like sound, often associated with group unity or
    communication

-   Ooer -- moo-like sound made by infants in distress

-   Gek -- quick "aaack" indicating disturbance

-   Scream -- shrill, loud, high-pitched sound made when aggressive or
    fearful

> Other gestures that indicate a threat or aggression include brow
> raises that display white eyelids, yawns directed at a specific
> individual, hitting the ground or object rapidly (slapping), teeth
> grinding, and staring intently at another individual.
>
> Baboons travel and feed during the day and sleep in trees or cliffs at
> night for protection from predators. Being very good scavengers,
> baboons can survive in areas that other primates cannot. They spend
> about half of their waking hours looking for, processing, and eating
> food. They may dig up roots and eat insects, lizards, small mammals,
> and even crabs or fish if near water. In captivity, they spend more
> time in social interaction and much less time feeding. Captive baboons
> can be fed a complete, commercially available diet, supplemented with
> a variety of other fruits and vegetables.
>
> **Mating and Reproduction**
>
> The female's skin on her rump, or perineal area, swells greatly
> according to her menstrual cycle. This is usually referred to as sex
> skin. Hamadryas females have a particularly large sex skin swelling.
> During the period of maximal swelling, she will ovulate and be most
> receptive to mating. The sex skin becomes flat and takes on a bright
> red or purple hue when she becomes pregnant. Gestation lasts from 18
> to 24 weeks. Infants are born black with pink faces and bottoms. They
> need the mother's protection, milk and transportation to survive. At
> about four to six months, the infant begins to change to the color of
> the adults. They are generally weaned by colony managers around five
> to six months of age, and although the natural weaning process will
> vary among baboon species, it generally occurs between one to two
> years of age. They become sexually mature at about three to five
> years.
>
> Social World
>
> Baboons live in a strict society. They clearly know their rank in the
> group and the rank of others, and behave toward others as appropriate
> for their dominance status. Baboons are very protective of infants and
> tolerant of juveniles, and males may carry and groom infants on
> occasion. Friendships have been reported between particular males and
> females.
>
> Baboons are incredibly social animals and should not be kept isolated.
> Infants should be kept with their mothers for at least a year to
> develop normal social skills. Compared to most other primates, baboons
> are fairly easy to put together into groups. Preferably, subspecies
> should be kept together, or at least in groups with similar structure
> as found in the wild, which can differ among and within species,
> probably based on the nature of the habitat in which the animals are
> found. Groups that combine a single male with multiple females are
> most common in captivity, but all-male groups also can be formed.
> Groups with multiple females and males are more difficult unless there
> is enough space for them to avoid aggression, especially fights over
> mates.
>
> Physical World
>
> **Housing**
>
> In general, baboons are quite hardy and adaptable. They can be
> successfully housed in a variety of captive conditions, from indoor
> cages to large outdoor semi-free ranging enclosures. Sturdy cages are
> required because baboons are strong and will manipulate the cage a
> great deal. Cages should be constructed to prevent the baboons from
> pulling off pieces of the cage and eating them. Baboons favor high
> perches. While some facilities have successfully used old tires and
> ropes for resting areas and swings, others have reported that the
> baboons eat the items and become sick. Alternative swings and resting
> areas can be constructed from metal or polyvinyl chloride. Large areas
> and/or visual barriers are necessary so that low-ranking individuals
> can avoid others. If aggression within the group is a problem,
> elevated resting areas or hiding areas should be added to help
> mitigate the aggression.
>
> **Enrichment**
>
> Feeding is a popular enrichment activity for baboons, who are very
> motivated by food. Due to their strict dominance hierarchy, only the
> most dominant male and female may eat food items provided to a group.
> To avoid this type of monopolization, it is best to scatter smaller
> food items all around the enclosure. In addition to feeding
> commercially available, nutritionally balanced diets, baboons can be
> offered food enrichments such as grains, fruits, vegetables,
> vegetation, bark, coconuts, peanut butter, dry fruit, honey, candy,
> cereal. The feeding of treats should not compromise the baboon's
> appetite for the nutritionally balanced food, so the quantity of
> treats provided should be monitored closely. Baboons will also ingest
> items that are not healthy for them, such as rocks, wire, metal or
> other harmful materials. Bloat has been reported if baboons eat too
> many orange peels or gas-producing vegetables (e.g., broccoli), and
> they may become impacted if they eat too much hair, hay or wood.
>
> Objects containing food must be heavy or they will be destroyed
> quickly. Puzzles made of sturdy materials, such as polyvinyl chloride
> (PVC), can be filled with treats. Toys on short chains can be coated
> with honey and dipped in grain, then frozen and hung on the cage, for
> a treat. Once the baboons eat the food, they can then play with the
> toy that remains. Frozen blocks of juice or water with fruit inside
> can be given to the baboons in the cage or enclosure, or hung from the
> roof with a chain. Locking nuts are necessary so the baboons do not
> unscrew the devices. Also, sturdy clips should be used to attach the
> device, and puzzles should be removed when empty to keep the baboons
> from breaking them.
>
> Since baboons manipulate and chew many objects, very sturdy dog toys
> make good baboon toys (e.g., rigid plastic balls; large, thick rubber
> toys; hard nylon dog chews). Hard, nontoxic logs or wood pieces can be
> used for chewing and even as perches. Pieces at least two to three
> inches in diameter are best so that they are not immediately
> destroyed. Wood items must be replaced on occasion and should be
> monitored so that large pieces or slivers do not endanger the baboons.
>
> Other types of enrichment include videotapes, mirrors, and wind
> chimes, which are especially helpful enrichment for singly caged
> baboons. Several commercially available enrichment items, including
> fleece boards made for grooming and plastic balls with holes in them
> and filled with treats, are not as useful for baboons and probably not
> worth the expense.
>
> New items may receive a lot of attention, but baboons will quickly
> tire of them. Replacement of toys or devices at regular intervals is
> important to keep the animal's interest high.
>
> Special Cases
>
> Older animals usually will become more isolated from the troop, but
> not always. Since they can't climb as well as their younger
> counterparts, they should have plenty to do at ground level. Food and
> water must be accessible near the floor, and food will have to be
> softened by soaking in water if the older baboon has lost some teeth.
>
> Infants are curious creatures and will explore any opening. It is
> essential to make sure that all possible openings are covered to
> prevent entrapment or escape.
>
> Problem Behaviors
>
> Like other monkeys, baboons can develop problem behaviors for a number
> of reasons. Being taken away from the mother and raised by humans is a
> major cause of later abnormal behavior patterns, as the infant must
> learn to cope with the loss of the mother and grow up in an artificial
> environment. Boredom, stress and, ultimately, problem behavior may
> result from confinement in small enclosures, lack of enrichment
> activities, solitary housing, or housing that does not afford the
> animal ways to avoid more dominant individuals or frightening
> situations.
>
> Examples of abnormal behavior patterns to watch for are hair eating
> and regurgitation. Extra feeding with food or "toys" can help to
> alleviate these behaviors that are related to boredom and not enough
> time spent feeding. Orphaned baboons often develop self-directed
> behaviors, such as self-sucking and clinging. They need appropriate
> attachment figures if they cannot be kept with the mother. One
> possibility is a mobile surrogate made of fleece-wrapped, three-inch
> PVC hung from the top of the cage. Exposure to peers or other friendly
> adults is critical to the orphan for normal development. It is very
> difficult to eliminate problem behaviors developed during infancy, but
> some individuals may be helped by gradually introducing them to
> friendly, perhaps younger, social partners.
>
> More severe problems, such as self-biting, also have been reported in
> captive baboons. Intensive efforts are required to reduce or eliminate
> this problem. A daily program of enrichment, with documentation of
> items that seem to reduce the frequency of self-biting is required and
> may need to be continued for the life of the baboon. For individuals
> that increase self-aggressive behaviors when new enrichment items are
> provided, enrichment provided outside of the cage (such as in
> association with positive reinforcement training) can be more
> effective until the behavior is under control. Abnormal behaviors in
> baboons housed alone are greatly decreased when the animals are placed
> into social groups.
>
> Some baboons are also very aggressive to one another, causing problems
> when they are put into new groups. This "hyper aggression" is more
> common in males and difficult to control, and it may be necessary to
> try multiple different partners, including females or even juveniles.
> It is important to observe the individual to determine what sets off
> the aggression, since it may be related to commotion in the
> environment, feeding time, etc. This can help to indicate options that
> may reduce the behavior (e.g., moving to another cage, separating
> during feeding).
>
> It is far more humane for the baboon and less work for the person to
> keep abnormal behavior patterns from developing. This can usually be
> accomplished by doing two things. First, keep infants with their
> mothers for about one year. Second, house baboons in social groups in
> large enclosures with enrichment to occupy their time.
>
> Safety Issues
>
> While they may have a reputation for being aggressive due to their
> size and large canines, baboons actually are mild-mannered and easy to
> work with compared to other primate species. They have elaborate
> threat displays that help to keep the peace in large groups, but
> actual aggression resulting in injury is not common. Given the size of
> baboons, it is not easy to "force" them into doing something, such as
> moving into a new cage. Greater success and a better relationship will
> develop if the baboons are treated with respect and positive
> interactions -- and they will respond with cooperation and friendly
> behavior.
>
> Baboons can be trained with positive reinforcement to cooperate during
> a variety of management procedures, including transferring them to new
> areas, getting them to show parts of their body for inspection, and
> performing certain medical tests (i.e., blood pressure measurement).
> Given their keen interest in food rewards, ability to learn quickly,
> and generally relaxed attitude around humans, they make good pupils.
> People can maintain positive interactions with baboons by providing
> treats to the baboons and taking care not to frighten them by staring
> at them or moving suddenly.
>
> Baboons should be sedated during physical examinations and other
> procedures that require physical handling, especially if they weigh
> more than about 11 to 15 lbs. The best way to move them is via a
> system of chutes and doors.
>
> References
>
> Altmann J. 2001. *Baboon Mothers and Infants.* Chicago: University of
> Chicago Press.
>
> Brent L, Koban T, Ramirez S. 2002. Abnormal, abusive and
> stress-related behaviors in baboon mothers. *Biol Psychiatry*
> 52(11):1047-56.
>
> Brent L, Belik M. 1997. The response of group-housed baboons to three
> enrichment toys. *Lab Anim.* 31(1):81-5.
>
> Brent L, Weaver D. 1996. The physiological and behavioral effects of
> radio on singly housed baboons. *J Med Primatol.* 25(5):370-4.
>
> Easley SP, Coelho Jr. AM. 1991. Is lipsmacking an indicator of social
> status in baboons? *Folia Primatol* (Basel) 56(4):190-201.
>
> Fortman JD, Hewett TA, Bennett BT. 2002. *The Laboratory Nonhuman
> Primate.* Boca Raton, FL: CRC Press.
>
> Kessel A, Brent L. 2001. The rehabilitation of captive baboons. *J Med
> Primatol.* 30(2):71-80.
>
> National Research Council. 1998. *The Psychological Well-Being of
> Nonhuman Primates.* Washington, D.C., National Academy Press.
>
> *Primate Lit: A Bibliographic Database for Primatology.\
> *http://primatelit.library.wisc.edu
>
> Rowe N. 1996. *The Pictorial Guide to the Living Primates.* East
> Hampton, NY: Patagonias Press.
>
> Smuts B. 2001. Friendship between the sexes: forming enduring
> relationships in an olive baboon troop. In *The New Encyclopedia of
> Mammals,* edited by D. MacDonald, 360-361. Oxford, England: Oxford
> University Press.
>
> Common Names of the Baboons
>
> *Papio anubis* or *P. hamadryas anubis*: Olive baboon, Anubis baboon
>
> *P. cynocephalus* or *P. hamadryas cynocephalus*: Yellow baboon,
> Savanna baboon
>
> *P. hamadryas* or P*. hamadryas hamadryas*: Hamadryas baboon, Sacred
> baboon
>
> *P. papio* or *P. hamadryas papio*: Western baboon, Guinea baboon
>
> *P. ursinus* or *P. hamadryas ursinus*: Chacma baboon
>
> Capuchins
>
> Background
>
> **Habitat**
>
> Flexibility, opportunism, and adaptability are the hallmarks of
> capuchin success. These monkeys occupy virtually every type of
> Neotropical forest, including humid and dry tropical forests, swamp
> forests, seasonally flooded forests, mangrove forests, and gallery
> forests, as well as dry, deciduous forests where rainfall is absent
> for five to six months of the year. They range from sea level forest
> to cloud forest up to 2700 meters above sea level. Capuchins are
> mostly seen in the middle layers of the forest, but will use all
> levels from the canopy to the understory, going to the ground to
> drink, forage or travel.
>
> **Physical Features**
>
> Capuchin monkeys weigh from six to 12 pounds and can live for more
> than 50 years. They are physically different from other New World
> Monkeys (platyrrhines) in that they have robust jaw and dental
> structures, large brains in relation to their body size, and
> moderately prehensile tails. Additionally, their hands have strong
> grips, a degree of opposition of the thumb to index finger, and
> somewhat independent finger movements. Taken together, these features
> afford capuchins a wide range of locomotor and foraging actions.
>
> **Behavior**
>
> Capuchins are active monkeys, agile at climbing and leaping. They use
> their hands and mouths to explore objects and surfaces, often
> destroying them in the process. More than other monkeys, capuchins act
> on their world through coordinated actions of hands, mouth, feet, and
> tail. They touch, handle, rub, bite, pull, push and pound objects as
> they explore them and manage to undo latches, untie ropes, unsnap
> hooks, and unscrew bolts.
>
> Endowed with unusual tendencies to combine objects and string together
> sequences of actions with objects, capuchins can, for example,
> successfully order a set of nesting cups. They can use their bodies in
> innovative ways, such as holding multiple cups with their hands and
> feet while working with them.
>
> Capuchin monkeys' memory and visual perception are similar to those of
> other nonhuman primates. They travel efficiently through familiar
> spaces from one location to another and they can use landmarks to
> locate objects they cannot see. They have good memories for
> significant events, and they perceive objects, object movements, and
> surfaces in much the same way as humans do.
>
> Capuchins are like other monkeys in that they can recognize an
> abstract relation among objects (e.g., sorting objects by size).
> Capuchins also can recognize two relations at the same time and use
> them in a nested or hierarchical fashion, such as sorting pictures by
> shape and sorting pictures of a given shape by size.
>
> It is important to note that captive monkeys cannot solve everyday
> problems that wild monkeys can without extensive practice. Individual
> experience and immediate context powerfully affect capuchins'
> problem-solving skills and exploratory activities.
>
> Capuchin monkeys express interest in other animals (including human
> companions) by looking at them, making facial expressions and
> vocalizing in specific ways to express different emotions, and
> touching them. Young monkeys cling to their companions. Adults
> occasionally groom their companions when they feel comfortable and
> relaxed, using hands and tongues to touch the skin or hair. They are
> also quite playful, especially young monkeys. Capuchins of any age
> tend to be docile, but can become aggressive, even toward human
> companions, if frustrated or frightened.
>
> **Mating and Reproduction**
>
> Capuchins reach sexual maturity at four to five years of age. Females
> have a menstrual cycle of 19 -- 22 days. Gestation lasts from 22 to 23
> weeks, followed by 22 weeks without menstruation during nursing if the
> mother rears the baby, or about seven to eight weeks without
> menstruation if she loses the baby. Infertility while nursing lasts
> months longer, even after menstrual cycling resumes.
>
> Female tufted capuchins (*Cebus apella*) display their interest in
> mating using a rich and varied behavioral repertoire consisting of
> facial expressions, vocalizations, gestures, and body postures. In
> general, the female actively follows a target male, which, in most
> cases, is the dominant male in her group. She directs most if not all
> of her solicitations toward this target male. Initially (for hours
> and/or days), the sought-after male does not reciprocate and tends to
> avoid the female by leaving as soon as she approaches him. Later, the
> target male starts to respond to the female's solicitations with
> behaviors similar to hers. At this point, mutual sexual interest
> becomes evident and mating occurs. Females of other species of
> capuchins express their interest in mating less overtly. In these
> species, solicitations of the female by the male may be more obvious
> than the female's solicitations of the male.
>
> Social World
>
> Capuchin monkeys in the wild live in groups throughout their lives.
> Males, females, and immature animals travel, feed, and sleep near one
> another every day. If a monkey loses sight of its group, it calls
> loudly and searches actively to find the group again. In captivity,
> capuchin monkeys live compatibly in pairs or groups, but they do not
> live happily alone. Spending any amount of time by themselves, without
> familiar companions, is a hardship for capuchin monkeys. Capuchins can
> live compatibly with other species, for example, squirrel monkeys.
>
> It is easiest to place capuchins in groups when they are young (three
> years old or less). Groups may range from pairs to two dozen or more
> animals, of mixed ages and sexes. Adults can live together in pairs
> compatibly, and pairs can be formed when animals are adults. Both male
> and female same-sex pairs are compatible, as are opposite-sex pairs.
> However, in the case of male-female pairs, one should make sure that
> the male does not monopolize food or other resources by virtue of his
> greater size and strength.
>
> Introducing adults to each other as pairs or one adult into an
> existing group should be done with careful supervision, because the
> monkeys may injure one another through fighting. Introducing an adult
> male to a group with a resident adult male is not advised. Allowing
> monkeys to get to know one another in a space where one can escape or
> hide from the other until they are comfortable together makes the
> introduction process safer. For example, one can place the newly
> introduced individual in visual contact with the group but in a
> separate cage for several days. The new individual can be placed
> closer to the group in a gradual manner. If all individuals behave
> calmly at this point, the newcomer's cage can be placed next to the
> group's cage, permitting some physical contact through wire mesh, for
> example. When the newcomer is not threatened by group members, open a
> doorway between the two. Permit the newcomer to enter the group
> voluntarily, and leave the release cage in place for a period of days
> so that the newcomer can return to it (i.e., escape from the group) if
> need be. There is no certain way to prevent fighting between members
> of a group and a newcomer, so all introductions must be carefully
> monitored.
>
> Physical World
>
> Capuchin monkeys in the wild spend most of their time in trees. They
> spend about half of their waking hours foraging, eating a wide variety
> of plant and animal foods. In captivity, providing opportunities to
> travel and rest above the ground promotes healthful exercise and
> hygiene. Providing perches at two or more heights allows capuchins to
> move around in a way that is natural for them. In general, the
> vertical dimension appears more important to these monkeys' use of
> space than the horizontal dimension.
>
> Capuchin monkeys benefit from additional opportunities for manual
> activities similar to those used in foraging, including manipulative
> puzzles and objects to handle and tear apart. Supplying a variety of
> objects, such as soft plastic items or cardboard, on a regular basis
> promotes healthful manual activity. Provision of these items must be
> monitored to ensure that gastrointestinal obstruction does not result.
> Providing a variety of foods, including different kinds of fruits and
> dairy products in addition to a commercial pelleted chow, is another
> element of good physical care. Fruits, seeds, nuts and eggs can be
> provided whole or minimally processed; cracking, peeling, separating,
> and otherwise processing food is healthful activity for capuchins, so
> long as they have the teeth and fingers to achieve this. Foods, such
> as peanut butter and honey, can be hidden in sections of a PVC pipe or
> a box with holes, and the monkeys will use straw or sticks to retrieve
> it. Monkeys new to these tasks may take some time to figure out how to
> solve these problems. Caregivers can provide "hints," such as placing
> the stick into the tube, to help them learn. It should be noted,
> however, that food treats should not be fed in such quantities to
> discourage the animals from eating their nutritionally balanced diet.
>
> As suggested by the wide variety of habitats in which they live,
> capuchin monkeys are fairly hardy with respect to temperature and
> humidity, although they cannot cope with freezing temperatures.
> Monkeys that are accustomed to a narrow range of temperatures and
> humidity should be introduced gradually to new conditions to give them
> time to acclimate. It should not be assumed that animals will
> spontaneously seek out heated indoor spaces when the outdoor
> temperature falls, especially if they have just arrived in new
> housing. Particularly if the ambient temperature falls below 68
> degrees Fahrenheit, perches and shelves should be constructed of
> materials that do not conduct heat quickly. Polyvinyl chloride (PVC)
> and wood, for example, do not conduct heat as quickly as metal.
>
> If outdoor temperatures drop below 45 degrees Fahrenheit, capuchins
> need access to a heated indoor enclosure. Optimum temperature ranges
> vary among the different species, but range from approximately 65-85
> degrees Fahrenheit. Infants and young juveniles need a heated space at
> even warmer temperatures. Cold monkeys sit in a huddled position with
> the tail wrapped around the body and move less frequently than normal.
> If there is snow on the ground, monkeys may walk in it voluntarily;
> this can quickly lead to frostbitten fingers and tails, which require
> amputation.
>
> Capuchins should have enough space to move in a normal manner by
> walking, climbing, and jumping, and places to sit that permit the tail
> to hang below the perch without touching the floor. They prefer to
> spend most of their time well above the floor and flee upward if
> frightened. However, they will spend much time manipulating a loose
> floor covering, such as straw or wood shavings. Such bedding materials
> provide an attractive focus for activity for captive monkeys and
> enrich the environment in a positive way.
>
> Capuchins housed in social groups, particularly if the groups are
> large (i.e., 10 or more monkeys), should have enclosures with at least
> two separate compartments, separated by a wall and with one or more
> connecting doorways or tunnels. This arrangement reduces injuries by
> permitting animals to avoid one another, and it makes separating
> animals simpler for the keeper and less stressful for the monkeys.
> Capuchins in exhibits such as zoos should have an area available to
> them that is away from the visitors' view, to allow for occasional
> privacy.
>
> Special Cases
>
> There are no particular considerations for older monkeys so long as
> they are in good health. Infants, on the other hand, require more
> frequent feeding, a more easily chewed and digested diet, and an
> object to which they can cling, such as a paint roller attached to a
> base so that it is stable and can be removed for washing. Even more
> than adults, infants need constant social companionship.
>
> Housing animals individually should be avoided. Extra provisions for
> manipulative activity should be provided for monkeys that are
> temporarily housed individually for medical or research reasons, but
> solitary activities do not substitute for social companionship.
>
> Problem Behaviors
>
> Noticeable changes in posture, movement, and activity level are
> indicators that a monkey may be ill. Capuchin monkeys can develop
> stereotypical movement patterns, such as pacing, and they may perform
> these more persistently when stressed. When captive monkeys
> persistently make vocalizations known as "chucks" that are used in the
> wild when predators appear, this means that they are frightened.
> Monkeys normally give chucks when strangers or people associated with
> capture, such as veterinarians, appear. Altering care routines or
> housing arrangements may reduce fear; social companions and
> alternative activities can help capuchin monkeys return to a calmer
> condition.
>
> Capuchin monkeys engage in a highly distinctive, self-care behavior,
> known as anointing, in which they rub pungent and sometimes topically
> irritating plant or animal materials on their fur. Captive monkeys may
> do this with oranges, for example. They also rub their bodies with
> urine, a behavior called urine washing. Although these behaviors may
> appear aberrant, they are, in fact, normal.
>
> Safety Issues
>
> Capuchins do not readily accept physical restraint, such as being held
> in a gloved hand. They will bite if frightened, as during restraint or
> imminent capture, and they have a strong bite. It is best to use a
> sturdy box with a latching sliding door to transport animals or to
> train them to participate voluntarily (e.g., using a leash and
> collar). Capuchins can be readily trained using positive reinforcement
> to perform behaviors required for many routine care procedures, such
> as moving from one place to another. Chemical or physical restraint
> should be a last resort only.
>
> As with all monkeys, handlers should be careful about latching cages
> securely. Capuchins are particularly interested in opening latches;
> mere springs or harness snaps, for example, will not hold them for
> long. A padlock is more secure.
>
> Capuchin monkeys are hardy when kept in healthful conditions. They
> are, however, highly susceptible to the common human cold and other
> respiratory illnesses. People suffering from these illnesses should
> not go near the monkeys. Like other monkeys, capuchins also are highly
> susceptible to measles, chicken pox, and other viral diseases common
> in humans. Capuchins (primarily *Cebus apella*) may be particularly
> susceptible to Type II diabetes if fed improperly and not allowed
> sufficient physical activity.
>
> Resources
>
> Bayne K, Dexter S, Suomi S. 1991. Ameliorating behavioral pathology in
> *Cebus apella* monkeys with social housing. *Laboratory Primate
> Newsletter.* 30(2):9-12.
>
> Cooper MA, Thompson RK, Bernstein IS, et al. 1997. The integration of
> stranger males into a group of tufted capuchin monkeys (*Cebus
> apella*). *American Journal of Primatology* 42:10 (Abstract).
>
> Fragaszy D, Visalberghi E, Fedigan L. 2004. *The Complete Capuchin:
> The Biology of the Genus Cebus.* New York: Cambridge University Press.
>
> Hayes SL. 1990. Increasing foraging opportunities for a group of
> captive capuchin monkeys (*Cebus capucinus*). *Laboratory Animal
> Science* 40:515-519.
>
> Ludes E, Anderson JR. 1996. Comparison of the behaviour of captive
> white-faced capuchin monkeys (*Cebus capucinus*) in the presence of
> four kinds of deep litter. *Applied Animal Behaviour Science*
> 49:293-303.
>
> National Research Council. 1998. *The Psychological Well-Being of
> Nonhuman Primates.* Washington, DC: National Academy Press.
>
> Nowak R. 1999. *Walker's Primates of the World.* Baltimore, MD: The
> Johns Hopkins University Press.
>
> Riviello MC. 1995. The use of a feeding board as an environmental
> enrichment device for tufted capuchin monkeys (*Cebus apella*).
> *Primate Report* 42:23-24 (Abstract).
>
> Visalberghi E, Anderson JR. 1999. Capuchin Monkeys. In: *The UFAW
> Handbook on the Care and Management of Laboratory Animals, Seventh
> Edition.* UFAW \[Universities Federation for Animal Welfare\] (edited
> by T Poole and P English), 601-610. Blackwell Science, Oxford, UK.
>
> Westergaard GC, Fragaszy DM. 1985. Effects of manipulatable objects on
> the activity of captive capuchin monkeys (*Cebus apella*). *Zoo
> Biology* 4:317-327.
>
> Common Names of Capuchins
>
> *Cebus albifrons ssp*: White-fronted capuchin, Brown-faced capuchin,
> Ecuadorian capuchin, Shock-headed capuchin, Trinidad white-fronted
> capuchin, Varied capuchin, Andean white-fronted capuchin
>
> *C. apella ssp*: Black-capped capuchin, Guianan brown capuchin, Brown
> capuchin, Tufted capuchin, Hooded capuchin, Large-headed capuchin,
> Margarita Island capuchin, Peruvian tufted capuchin
>
> *C. capucinus ssp*: White-throated capuchin, White-faced capuchin,
> Panamanian white-throated capuchin, Gorgona white-fronted capuchin
>
> *Cebus libidinosus ssp*: Bearded capuchin, Tambopata tufted capuchin,
> Pale capuchin, Paraguayan tufted capuchin
>
> *C. kaapori*: Ka'apor capuchin
>
> *C. nigrivittatus ssp*: Weeper capuchin, Weeping capuchin,
> Black-horned capuchin, Crested capuchin
>
> *C. olivaceus ssp*: Brown weeper capuchin, Chestnut capuchin, Ka'apor
> capuchin, Kakapo capuchin, Wedge-capped capuchin, Weeper capuchin,
> Weeping capuchin
>
> *C. xanthosternos*: Yellow-breasted capuchin
>
> Chimpanzees
>
> Background
>
> **Habitat**
>
> In the wild, chimpanzees live in large forested areas, but they may
> also inhabit dry savannah and mosaic habitats of
> grassland-woodland-forest environments, as well as montane forests up
> to 10,000 feet in elevation. They spend much time in trees and may
> scatter widely over their territory rather than traveling around in
> one large group.
>
> **Physical Features**
>
> Chimpanzees weigh up to 200 pounds, though the normal average weight
> for an adult female is 130 pounds and for an adult male is 140 pounds.
> Chimpanzees may grow to a height of 3 - 5 1/2 feet. Adult males
> generally are larger than females. Reaching their adult size by the
> time they are 14 to 16 years old, these animals can live to be 60
> years old, with an average life span of 40 to 45 years. Chimpanzees
> are extremely strong and quick. They are omnivores, eating fruits,
> vegetables, insects and other animals at times.
>
> **Behavior**
>
> Chimpanzees have many ways of communicating with each other. Facial
> expressions, calls, and gestures reflect their relationships with
> other chimpanzees and with people. Understanding these methods of
> communication is essential for having a good relationship with them
> and staying safe in their presence.
>
> Chimpanzees make noisy shows of banging, hooting, rocking back and
> forth, and running, hitting or kicking things as they go. This is
> called a "display" and is normal for them. They do this because they
> are excited or trying to impress. Displays are common when chimpanzees
> meet new chimpanzees or people and at the arrival of food. Sometimes
> chimpanzees will throw feces or spit on people during these displays.
> Reacting to such behavior (e.g., jumping away, yelling at the
> chimpanzee) will only encourage it. Walking away slowly or ignoring
> this behavior will discourage it over time.
>
> It is important to recognize that there is a hierarchical priority
> among chimpanzees for access to food that must be considered during
> feeding, foraging activities and access to enrichment foraging
> devices. Chimpanzees may show their lower status to another chimpanzee
> by bowing or grunting.
>
> Chimpanzees make different sounds and expressions depending on what
> they are doing and trying to communicate. They may make a series of
> small grunts as they eat and a call that sounds like "WHA-OOO" as a
> warning of possible danger. If frightened or nervous, they will show
> their teeth and gums. Alternately, when playful, chimpanzees may show
> a wide-open mouth with the top teeth covered. They also make snorting
> or panting sounds when they play. Other gestures/vocalizations include
> an "open mouth grimace" (to express fear), squeal and pant-hoot (to
> express excitement).
>
> An angry chimpanzee will press its lips together tightly, a warning to
> stay out of reach. Chimpanzees threaten each other by gesturing
> forward violently with an arm or wrist, as if shooing another away.
>
> Friendly contact is extremely important to them. Chimpanzees will
> spend long periods of time grooming each other or simply sitting in
> contact. Many chimpanzees are very playful as well, tickling, chasing,
> wrestling, and gnawing on each other.
>
> **Mating and Reproduction**
>
> Puberty starts at about seven years of age. Male chimps can breed as
> young as seven to eight years of age. Female chimps in captivity can
> get pregnant as young as nine years of age. Because menopause is not
> documented in chimpanzees, females can remain fertile for decades.
> Females in estrus, which happens every four to six weeks, have
> prominent swelling of the pink genital skin that usually lasts two
> weeks. When in estrus, they may mate many times a day if housed with a
> male. There is no breeding season. Chimpanzee pregnancy lasts 33 to 34
> weeks. Newborns cannot hold on to their mothers, who need to support
> them so they can nurse. Infants should be able to cling to their
> mothers without help after a few days. After several months, infants
> may start riding on their mothers' backs rather than abdomens. Infants
> will nurse until they are about three years old.
>
> Social World
>
> In the wild, chimpanzees live in large social groups. These groups
> share a territory and are hostile to other groups. Typically, a wild
> chimpanzee will know many other individuals, visiting with them on a
> regular basis. While wild chimpanzees often spend part of the day
> alone, they are naturally social animals for whom constant solitude is
> a hardship.
>
> In captivity, housing chimpanzees in social groups is essential to
> their quality of life. Young animals learn many lessons from the
> other, older animals in the group.
>
> However, it is not always easy to form and maintain such groups. One
> must take great care in introducing unfamiliar chimpanzees to each
> other, keeping in mind that they are hostile to strangers in the wild.
> Several steps can be taken to make introductions go more smoothly.
> First, it is a good idea to let chimpanzees see but not touch each
> other for a short amount of time. Long periods of seeing but not
> touching, however, may make them more hostile to each other. Ideally,
> giving them a day or two of seeing each other should be followed by
> letting them touch each other but not enter each others' enclosure.
> This gives them a chance to meet each other and establish dominance
> more safely than suddenly putting them together in the same enclosure
> as complete strangers.
>
> Some fighting during introductions is not unusual. A few fights, even
> those that cause small wounds, are not necessarily cause for
> separation. The animals need time to establish a hierarchy. It is
> important to give them time to work this out and reconcile after
> fights, which they often do. However, if fights become more frequent
> or more severe over time, then the individuals may indeed be
> incompatible.
>
> Newly-introduced chimpanzees should be watched carefully for at least
> a week. It is important to keep things quiet and calm around them,
> since they will be more likely to attack each other when there is
> noise, commotion or a stranger nearby. If several chimpanzees are to
> be introduced into one group, it is best to introduce different
> combinations of pairs together over several days before putting
> everyone together. If a male and female are introduced to each other,
> the introduction will go more smoothly during the time of month when
> the female has a sexual swelling. The riskiest social introductions
> involve males meeting each other, or chimpanzees that were housed
> alone for long periods of time.
>
> Even chimpanzees that know each other well may fight on occasion.
> Fights often look and sound worse than they are. Trying to stop a
> fight, for example, by spraying chimpanzees with water, will do no
> good and may make things worse. Separating them and keeping them alone
> for a while is also a bad idea. They will remember their dispute and
> may fight even worse once they are reunited. It is best to let fights
> take their course unless they are likely to cause significant harm or
> are life-threatening. It is important to avoid unnecessary separations
> of chimpanzee groups, since they will often fight during reunions.
> Subtle changes in body movements and posture often signal that an
> aggressive encounter is about to take place, especially between males.
> The male may exhibit slow swaying movements, raising of hackles and an
> increase in the volume of hooting.
>
> While it would be difficult to eliminate all fighting, it is a good
> idea to avoid giving chimpanzees things to fight over, such as toys
> and food. Minimizing competition for food can reduce the number of
> fights. For example, giving a group one watermelon is much more likely
> to cause fighting than scattering pieces of watermelon all over the
> enclosure. Similarly, it is a better idea to give a group of
> chimpanzees several boxes to play with rather than one big piece of
> cardboard.
>
> In captivity, chimpanzees benefit from social interaction with people
> (conducted safely), particularly when they lack companions of their
> own species. Many captive chimpanzees will want to groom humans, be
> groomed, or play chase or tickle games. While friendly relationships
> with people can be essential to chimpanzees with few or no companions,
> there are significant, potentially lethal, physical risks to people
> associated with such interactions (e.g., bite wounds, scratches,
> bruising, and possibly the transmission of infectious diseases), and
> the best approach in most circumstances is the provision of another
> chimpanzee.
>
> Physical World
>
> In the wild, chimpanzees spend much time in the trees. Thus, in
> captivity, they need climbing structures and comfortable places to sit
> up high. Fire hose, strong chain, cargo nets, perches, and tire swings
> all can be used for this purpose. If rope or chain is used, it should
> be thick and taut enough to prevent loop-forming and possible
> strangulation. Structures that provide shade and privacy, such as
> concrete culverts and small lengths of solid fencing, help avoid
> overheating in hot weather. They also give chimpanzees solitude if
> they want it and help to reduce aggression by providing visual
> barriers. Movable structures such as empty plastic barrels are favored
> resting spots, and chimpanzees can move them to where they want to
> sit. Barrels cut in half are popular "toys" for chimpanzees.
> Enclosures that include an outdoor area will provide the opportunity
> for chimpanzees to engage in the normal variety of behaviors typical
> for the species. Letting them choose whether to be inside or outside
> is important, since it appears that chimpanzees like to make some
> decisions for themselves.
>
> Wild chimpanzees build nests out of branches and leaves. When caged,
> chimpanzees will benefit greatly from having nesting material such as
> blankets, straw or hay (though these materials may be allergenic),
> etc. Tree branches may be used, although be aware that some common
> trees, such as fruit trees, magnolia, some oaks, and hickory are
> toxic. Care also must be taken to avoid providing branches that are
> long enough for chimpanzees to use them to escape from open-top
> enclosures. In large enclosures, entire uprooted trees have been
> provided for enrichment.
>
> One relatively easy way to keep life interesting for chimpanzees is to
> give them a large variety of healthy foods over time. While the basis
> of the diet (e.g., commercially prepared feed) should be nutritionally
> complete, fruits and vegetables, breakfast cereal, eggs, yogurt and
> other healthful snacks are good supplements. These are best provided
> as frequent, small feedings, rather than in large quantities once a
> day. While it is important not to overload chimpanzees on food treats,
> a sprinkling of "snacks" can help to prevent boredom and abnormal
> behaviors, particularly if the animals have to move around the
> enclosure to obtain the snacks (i.e., work for them). In the wild,
> chimpanzees rarely go very long without eating, regularly snacking on
> ripe fruits and leaves. Also, the more time-consuming the food is to
> find and eat, the better it is for the chimpanzee. Foods such as
> unshucked raw ears of corn and frozen, finely chopped and widely
> scattered foods help keep chimpanzees occupied. Requiring chimpanzees
> to climb by placing frozen items on wire mesh ceilings or elsewhere
> presents a challenge for them and provides exercise.
>
> Another easy way to enrich the chimpanzee's environment is to provide
> large, sturdy toys that are sold for children, large dogs and zoo
> animals. Many vendors sell toys at a lower price than at the local pet
> store. Rotating toys will maintain the interest of the animals.
> Providing climbing structures is especially important.
>
> Chimpanzees like to destroy things. Giving them items they can safely
> wreck, many of which are free or very inexpensive, is a widely used
> way of entertaining them. A cardboard box can be played in, squashed,
> ripped, chewed, and finally used for nesting material. Long sheets of
> butcher paper are very entertaining (butcher paper is easier on drains
> and easier to clean up than newspaper). An empty plastic soda or milk
> bottle, perhaps containing a small food treat, provides a good source
> of entertainment. Such objects, however, must be checked frequently
> and removed when they become damaged. Because small objects can lodge
> in the throat or other part of the intestinal tract, objects
> introduced for enrichment purposes must be monitored to ensure animal
> safety.
>
> Chimpanzees are extremely intelligent and will benefit from
> problem-solving and other mental activities. Inexpensive puzzles and
> projects can be made out of materials available at a home-improvement
> store. Even something as simple as a piece of polyvinyl chloride (PVC)
> pipe smeared on the inside with peanut butter, along with a stick or
> narrower piece of pipe to insert to get at the food, makes a pleasant
> diversion for chimpanzees. A PVC pipe drilled with a few finger holes
> and containing a frozen banana is another easy idea. Other safe and
> effective puzzles are described on the internet (see online resources
> listed at the end of the chapter.). Many chimpanzees enjoy finger
> painting or drawing with nontoxic crayons. Finally, training is great
> stimulation for the smart mind of a chimpanzee and is fun for people
> as well.
>
> Chimpanzees should be housed in an environment that gives them
> adequate ventilation, shade during hot days, and heat during cold
> days. Providing a fresh flow of air is recommended if the temperature
> gets as high as 90° F. They may enjoy the flow of water from a
> sprinkler placed outside their enclosure so that part (but not all) of
> their housing area receives some cooling. Chimpanzees should never be
> exposed to temperatures below 50° F. Even at higher temperatures than
> this, they will need supplemental heat.
>
> Special Cases
>
> **Age-related Considerations**
>
> Chimpanzees can live for more than forty years in captivity. During
> the course of their long lifespan, their needs change. Infancy is a
> critical time behaviorally and will determine whether the animal grows
> up to be behaviorally normal or have life-long behavior problems.
> Infants should remain with their mothers as long as possible. In the
> wild, young chimpanzees need their mothers' care until they are about
> five years old. Separation from the mother before the age of one or
> two will result in an adult that may have trouble getting along with
> other chimpanzees, show a lot of abnormal behavior, and not cope well
> with changes and stressors. If infants are reared apart from their
> mothers, exposure to other infant chimpanzees is critical.
>
> At the other end of the lifespan, the needs of chimpanzees change as
> well. Regular health care through a qualified veterinarian, important
> throughout a chimpanzee's life, is critical in old age. Aged
> chimpanzees experience many of the same problems that old people do,
> including bone loss, joint problems, and undesirable weight changes.
> Obesity increases the risks of cardiovascular disease and other health
> problems. Comfortable enclosures with bedding become particularly
> important. Aged chimpanzees can be expected to be less active, but
> their needs for a social life and stimulating environment do not
> diminish.
>
> **Individual Housing**
>
> A chimpanzee that must be individually caged due to health problems,
> severe social problems, the unavailability of social partners, or
> research reasons will require extra care in the form of enrichment and
> human interaction. While a chimpanzee may have to be individually
> caged, it should not be kept alone in a room, unless it is necessary
> to control the spread of disease. Rather, it should have visual and
> auditory contact with chimpanzees in other cages.
>
> All the enrichment ideas mentioned above are especially critical for
> the singly caged chimpanzee. Providing a more interesting diet is
> another way of reducing boredom, but the fact that individual
> chimpanzees tend to be inactive means that a lot of attention has to
> be paid to food quantities and calories to avoid obesity. Freezing
> fruits and vegetables, or scattering low-calorie items in straw are
> ways of increasing feeding time without adding too many calories.
> Singly caged chimpanzees will make a lot of use of toys and videotapes
> or live-feed of other chimpanzees (particularly familiar individuals).
> Very sturdy hand-held mirrors also may provide entertainment.
> Providing new structures or changing the installation of structures
> from time to time (e.g., suspending fire hoses in a new position) is
> another way to vary their environment and induce exploration
> behaviors. Access to the outside benefits all chimpanzees and provides
> a great deal of stimulation to singly caged chimpanzees.
>
> Problem Behaviors
>
> Captive chimpanzees may develop bad habits, including strange
> behaviors not normally seen in the wild. Some of these behaviors are
> very harmful to the animal's physical health. The most serious problem
> behavior is self-biting and self-wounding, collectively referred to as
> self-injurious behaviors (SIB). Little can be done about this behavior
> once the chimpanzee is in the habit of hurting itself, although there
> is some evidence with other primate species that pharmacologic
> intervention may control SIB. Such chimpanzees need intensive
> veterinary care and a strong behavioral management program for life.
>
> Other behavioral problems that are difficult to eliminate because they
> develop early in life can be reduced by enriching the chimpanzee's
> environment. Examples of these abnormal behaviors include rocking,
> thumb sucking, eye or ear poking, hair plucking, or odd and pointless
> motions or postures. Some of the easier abnormal behaviors to
> eliminate involve strange "eating" habits, such as consuming
> regurgitated food and feces. Increasing the number of small meals and
> providing bedding can help to eliminate such behaviors. Adding
> climbing structures and playthings also can be tried. Positive
> reinforcement training can be used not only to improve the quality of
> the chimpanzee's life but to train for behaviors that replace the
> problem behavior.
>
> Some problem behaviors may be due to physical rather than
> psychological causes. A sudden change in behavior or the development
> of a new abnormal behavior calls for a medical evaluation. For
> example, diarrhea may be a response to psychological stress, in which
> case changes to the environment might help. On the other hand, it
> could be the result of bacterial or parasitic infection requiring
> treatment.
>
> No one technique for dealing with problem behavior is foolproof. Each
> chimpanzee is an individual. A chimpanzee should be watched to
> determine the effectiveness of changes made. Several different
> approaches may need to be tried before a behavior problem improves.
> Some attempts to fix behavior may backfire as well, so familiarity
> with the individuals and ongoing observation is essential. For
> example, one chimpanzee may be unreasonably frightened of something
> new or different, while another will take to it immediately.
> Chimpanzees may adjust to something new gradually or avoid it forever.
> In some cases, the chimpanzee's immediate reaction is different from
> its long-term response. Observe the chimpanzee to see if it makes use
> of the enrichment, and if it reduces or eliminates the behavior
> problem. It is important to keep a record of what changes were made
> and how the chimpanzee responded.
>
> Safety Issues
>
> Chimpanzees are fast and strong, so great care must be taken when
> working with them. Chimpanzees that want to be groomed or tickled can
> press their backs or shoulders against enclosure mesh or bars for you;
> there is no need to stick your hand in the enclosure and risk getting
> bitten or grabbed. Indeed, some chimpanzees will appear to invite such
> contact, only to quickly turn and try to bite the person. Furthermore,
> always keep an eye on where their hands are and stay away from their
> mouths.
>
> Chimpanzees can be extremely unpredictable. They are known to trick
> people into coming within grabbing distance by pretending their arms
> cannot reach out as far as they actually can. If agitated, they may
> lash out at familiar people to whom they have never been aggressive
> before.
>
> Chimpanzees can certainly hurt people, and people can inadvertently
> expose the animals to harm. For example, chimpanzees can catch the
> same illnesses humans can, so care should be taken not to expose them
> to people with colds or the flu. Anyone working around chimpanzees
> should have a tuberculin test every six months or other documentation
> of being tuberculin negative (e.g., chest x-rays).
>
> An excellent way for people to interact more safely with chimpanzees
> is to utilize a training technique known as positive reinforcement, in
> which a desired behavior is linked to something the animal likes.
> People can positively reinforce chimpanzees by "catching" them doing
> something desirable (e.g., sitting down, leaning its shoulder against
> the enclosure barrier near you, etc.), and praising or treating them
> with a small food reward. By using a specific word or gesture when the
> chimpanzee performs the desired behavior, people can eventually use
> the word or gesture to "ask" for the behavior. Because such training
> takes some level of expertise, one should be familiar with positive
> reinforcement training techniques, both in general and specific to
> chimpanzees, before attempting this procedure.
>
> Chimpanzees can be trained to play with or groom each other or to stop
> stealing each others' food. Many chimpanzees enjoy learning a variety
> of commands (e.g., show me your shoulder, bring me your toy). While it
> may start as a game just to stimulate their minds and have fun, these
> commands may come in handy unexpectedly. For example, it may be
> possible to command an injured animal to present the body part for
> inspection. It may also form the basis for training chimpanzees to
> cooperate with procedures that would otherwise be very stressful for
> chimpanzees and people alike.
>
> Like all wild animals, chimpanzees will need to be restrained
> occasionally for clinical care and transport. However, chimpanzees can
> be trained to cooperate with procedures. Training can be used to make
> procedures such as receiving an injection or moving from the home cage
> to a transfer cage less frightening and stressful for the animal. A
> chimpanzee trained to cooperate with medical procedures such as heart
> rate or temperature measurement may not need to be anesthetized for
> those procedures.
>
> Positive reinforcement training should be employed whenever possible
> and will result in a positive relationship between chimpanzees and
> their caregivers. Letting chimpanzees know what is needed of them, and
> giving them a chance to cooperate, gives them some control over their
> lives. Threatening or punishing chimpanzees, on the other hand, will
> encourage them to do unpleasant things to people (spitting, throwing
> feces) and resist their caregivers at every opportunity.
>
> Resources
>
> Brent L (Ed). 1997. *The Care and Management of Captive Chimpanzees.*
> American Society\
> of Primatologists. 252pp.
>
> Maki S, Bloomsmith M. 1989. Uprooted trees facilitate the
> psychological well-being\
> of captive chimpanzees. *Zoo Biol* 8:79-87.
>
> Reinhardt V. 1997. The Wisconsin Gnawing Stick. *Animal Welfare
> Information Center\
> (AWIC) Newsletter* 7(3-4), 11-12.
>
> **Chimpanzees in the wild and in captivity:**
>
> http://www.discoverchimpanzees.org/chimps/chimps.php (Jane Goodall
> Institute Center\
> for Primate Studies)
>
> http://www.oaklandzoo.org/atoz/azchimp.html (Oakland Zoo)
>
> http://www.honoluluzoo.org/chimpanzee.htm (Honolulu Zoo)
>
> **Enrichment:**
>
> http://www.arkanimals.com/ark/e_enrichment_101.html
>
> http://www.awionline.org
>
> **Training:**
>
> http://www.awionline.org/Lab_animals/biblio/jo-6.htm
>
> http://behavior.org/animals/index.cfm?page=http%3A//behavior.org/animals/animals_chimps.cfm
>
> http://www.nal.usda.gov/awic/pubs/primates/4n4laule.htm
>
> **A useful listserv: ask questions and get answers, exchange ideas:**
>
> http://pin.primate.wisc.edu/infoserv/forums/pef/
>
> http://www.primate.wisc.edu/mailman/listinfo/pef
>
> **Primate Organizations:**
>
> American Society of Primatologists, www.asp.org
>
> Association of Primate Veterinarians, www.primatevets.org
>
> International Primatological Society, http://pin.primate.wisc.edu/ips/
>
> Common Names of Chimpanzees
>
> *Pan troglodytes*
>
> *P. troglodytes troglodytes:* Tschego
>
> *P. troglodytes verus:* Common or masked chimpanzee
>
> *P.troglodytes schweinfurthii:* Eastern or Long-haired chimpanzee
>
> *Pan paniscus:* Pygmy chimpanzee, Bonobo, Lesser chimpanzee
>
> Macaques
>
> Background
>
> **Habitat**
>
> The macaques represent a collection of approximately 20 species of
> monkeys, most of which are found in Asia. They occupy a wide
> geographic range that is considered second only to man in its extent.
> In this range, the habitat occupied by macaques varies from near
> desert to rainforest, and from sea level to snowy mountain tops. Some
> macaques spend the majority of their time in trees, while others are
> predominantly ground-dwellers. Many live in close proximity to human
> beings; the rhesus monkey is sacred to Hindus and is often found near
> temples in India and Nepal.
>
> **Physical Features**
>
> In general, the macaques have a medium-sized body, with a stocky
> build. Animals belonging to the smallest species weigh approximately
> 13 pounds, while representatives of the largest species weigh an
> average of 40 pounds. Tail length varies among the different species.
> All macaques have long, sharp canine teeth and finger nails that can
> pose a risk to human handlers through either bite or scratch wounds.
> They also have cheek pouches and a fully opposable thumb. The
> opposable thumb gives these animals the ability to manipulate objects
> (e.g., cage latches) with great precision. They feed on both animal
> and vegetable resources and have a highly varied diet. Macaques are
> primarily active during the daylight hours, and most species sleep in
> trees at night.
>
> Behavior
>
> As a rule, the macaques are social animals, living in groups of
> multiple males and females; the sex ratio typically reflects more
> females than males in a group. Even for the same species, group size
> tends to be smaller when the home range size is also smaller (e.g.,
> when constrained by human activities). Within these groups,
> individuals are ranked according to dominance (hierarchies), with the
> higher ranking animals doing more of the successful breeding and
> having first access to food and other desirable resources. Often it is
> the rank of the mother, rather than the father, that determines the
> rank of offspring. Young males may be evicted from their birth group
> as they approach puberty, forming temporary "bachelor" groups until
> they join a new group. Wounding of animals can occur when challenges
> for dominance occur.
>
> Because these animals rely in large part on visual communication, they
> use a number of facial signals, often accompanied by vocalizations, to
> threaten or to make friendly overtures. Threat displays include
> opening the mouth in the shape of an "O", a direct stare, raising the
> eyebrows quickly and repeatedly, flapping the ears, a jerky head-bob,
> shaking an object in their environment such as a tree branch or cage
> door, slapping the ground, or charging with intent to fight.
> Occasionally, a lack of compatibility between animals can be detected
> simply by the increased physical distance maintained between them.
> Behavioral indicators of compatibility between animals include social
> grooming, lip-smacking, and sitting in close proximity. Food sharing
> has also been used to assess compatibility between pairs of animals.
>
> **Mating and Reproduction**
>
> The reproductive cycle of macaques is characterized by a seasonal
> estrus period, with menstrual cycles occurring throughout the year.
> Females have been reported to begin cycling as early as approximately
> 1.5 years, although a more typical age is 2.5 years. Most species of
> macaques exhibit swelling and reddening of the skin of the rump,
> perineum, and occasionally arms, legs and face (referred to as "sex
> skin"). The swelling and reddening becomes more pronounced from
> beginning to end of the menstrual cycle. Exceptions to this are bonnet
> macaques and toque monkeys, who do not have marked sex skin. Menopause
> occurs in the macaques, with the number of menstrual cycles decreasing
> each year when the animal reaches her third decade of life.
>
> In general, the female actively solicits mating by the male (again,
> the bonnet macaque is an exception to this). Usually, the dominant
> males in the group breed the females more often, although less
> dominant males in a group have been reported to breed and reproduce
> successfully. The rhesus monkey's gestation period is between five and
> six months. The infant is quite dependent upon the mother, and the
> current preference is to leave the infant with its mother until
> approximately one year of age to help ensure adequate development of
> social, particularly maternal, skills by the developing infant.
>
> Social World
>
> Because of the intrinsic social nature of macaques, pair or group
> housing of compatible animals is extremely important. It is well-known
> that raising a macaque alone, without the company of other macaques of
> the same species, will result in that animal expressing a pattern of
> abnormal behaviors that can become self-destructive. Even the behavior
> profiles of adult animals housed alone can degenerate into inciting
> these abnormal behaviors, which may include repeated pacing, circling,
> or somersaulting; hyper-aggression; depression; and self-injurious
> behavior, including hair plucking or self-biting. (See section on
> "Problem Behaviors").
>
> While group or pair housing is strongly recommended for macaques, care
> should be taken in doing so. Since these primates establish dominance
> hierarchies and space is limited in captivity, the macaque wishing to
> flee the dominant animal has no place to fully escape. This can result
> in unresolved, increased aggression between the animals as well as
> wounding (and possibly killing) of one or more animals.
>
> Larger groups of animals that previously have been living in smaller
> stable cohorts should not be formed, because this will increase
> fighting between the smaller, pre-established groups. A better
> approach is to place unfamiliar animals together in a new enclosure at
> the same time. In this way, coalitions have not already been formed,
> and each macaque must establish its own place in the hierarchy without
> support from other animals.
>
> One approach to forming pairs of macaques is provided at the end of
> this chapter. The key steps include the following:

-   Introducing the animals into an area that they do not consider as
    their territory

-   Assessing facial expressions, postures and physical distance between
    the animals

-   Proceeding slowly in forming pairs

-   Planning ahead to have a way of separating animals should the
    fighting become intense (e.g., a panel to slide between cages, use
    of water, etc.)

-   Ensuring the safety of people performing the animal introductions

-   Providing ongoing monitoring of animal interactions, because animal
    relationships can change over time

> Using the natural social structure of the macaques will assist in
> forming compatible pairs or groups of monkeys. For example, because
> macaques will form bachelor troops, often males can be pair-housed
> successfully. Successful pairings of a young macaque with an older
> animal (so that the dominance hierarchy is clear and fighting is
> minimized) also have been reported.
>
> Physical World
>
> **Housing**
>
> Macaques have been housed successfully in a variety of types of
> housing, including island environments, corrals, corn cribs,
> indoor-outdoor runs, pens and cages. Regardless of the enclosure
> design or size, it must be sturdy enough to withstand being shaken and
> chewed on by its inhabitants. Because of the animals' tendency to flee
> upward when escaping a perceived threat, they benefit from perches,
> shelves or other structures that increase the three-dimensional space
> of the enclosure. Generally, older macaques prefer a non-moving shelf
> or perch, while the younger ones will readily use swings. Because
> macaques can strangle on lengths of chain, swings should be short in
> length and/or constructed of materials that cannot loop around the
> neck, such as flexible polyvinyl chloride (PVC) tubing. Similarly,
> ropes can be picked apart or chewed on, and this may result in a
> gastric obstruction. Thus, in most cases, ropes of cotton, sisal or
> jute should be avoided.
>
> In general, macaques should not be exposed to cold or wet weather
> without a method for them to conserve body heat. Japanese macaques
> living in the snowy mountains of Japan manage to stay warm by soaking
> in natural hot springs. A number of captive macaques, however, have
> lost parts of their tails or one or more digits to frostbite. This
> problem can be reduced or prevented by providing them with
> supplemental heating or a shelter.
>
> During conditions of high heat and humidity, macaques may overheat if
> they undergo a physical stress, such as being chased around an
> enclosure. Providing macaques with a shallow and indestructible pool
> in which to swim and cool off can be an asset to macaques housed
> outdoors in warmer climates. The swimming pool should be shallow, to
> prevent animals from drowning, and resistant to deterioration from
> chewing. The pool should be cleaned routinely to provide animals with
> good quality water for swimming.
>
> **Enrichment**
>
> The macaques are curious and intelligent animals. Providing them with
> opportunities to investigate and explore their environment is
> enriching for them. This can be accomplished by maintaining toys in
> the animals' enclosures. Since macaques have color vision, the toys
> (also known as manipulanda) should be of different colors; they can
> also be of different shapes and texture. Because the monkeys will chew
> on these toys, they should be relatively durable, such as heavy-duty
> dog toys. Toys should be removed from the enclosure when they become
> sufficiently damaged that the primate might swallow or choke on a
> piece. Rotating different toys in the enclosure and removing them
> periodically will help to keep the toys novel and increase the
> animals' interest in them.
>
> A very successful way to fulfill these animals' inclination to explore
> and investigate is to give them the opportunity to forage (or search)
> for food. Since many primates will spend up to 70% of their waking
> hours in foraging-related activities, offering captive primates the
> opportunity to engage in this behavior can be important in preventing
> the development of abnormal behaviors. Numerous in-house and
> commercially produced devices are available, including toys that
> simply hold the food item and require the monkey to fish for or push
> it out. Also available are containers with finger holes or slots
> through which the monkey removes the food item, as well as puzzle
> boards in which the monkeys must manipulate the food item though a
> maze before it reaches a hole large enough from which the food can be
> retrieved. Food may be hidden throughout the enclosure to encourage
> searching behaviors. Food items may also be ground up into small
> pieces or pre-purchased as "crumbles" and then placed on an
> Astroturf^®^ or artificial fleece foraging board. The small size of
> the food particle encourages manual dexterity and extends the amount
> of time the animal spends searching for and eating the food. Food
> treats, as enrichment, should not be offered in such quantity that the
> animal ignores its more nutritional daily diet or gains excessive
> weight. Many commercially available food treats come in a variety of
> flavors and are nutritious.
>
> Special Cases
>
> **Age-related Considerations**
>
> The macaques are long-lived animals, with reports of some animals
> living in captivity over 30 years. This lifespan entails a commitment
> of considerable duration, with substantial, changing needs of the
> animal over the course of its life. As with other species of primates,
> the design of the environment should take into account the age of the
> macaque. For example, older monkeys will develop arthritis, limiting
> their ability to jump onto perches, swing, or otherwise navigate their
> enclosure. Older primates can also have reduced vision capabilities,
> thus further limiting their ability to move around the enclosure and
> interact with other animals or people.
>
> Conversely, young animals are very active and curious. The enclosure
> design should allow them to express these characteristics without
> compromising their physical safety. Young animals also are
> particularly sensitive to the effects of social deprivation and should
> be housed with other primates of the same species whenever possible.
>
> **Individual Housing**
>
> The circumstance in which only one macaque is housed on the premises
> should be avoided. If several macaques are housed individually in
> cages, they should be able to see, hear and smell each other. If
> possible, individually caged animals also should have access to visual
> barriers in order to avoid being seen by other animals, should they so
> choose. It is recommended that if an animal cannot be socially housed,
> other forms of enrichment (e.g., toys, foraging opportunities) should
> be provided to compensate for the lack of social stimulation.
>
> **Susceptibility to Disease**
>
> Because of their close genetic relationship to humans, nonhuman
> primates can be susceptible to human diseases. Of particular concern
> is the exposure of macaques to tuberculosis from a human. Tuberculosis
> is a highly contagious, fatal disease in Old World Monkeys. Routine
> testing of the animals is highly recommended. Macaques are also
> susceptible to measles virus, and will show a rash similar to that of
> people having the disease. Most colonies of macaques are vaccinated
> for measles virus. Because numerous individuals may be assisting with
> the enrichment program (including volunteers), close attention should
> be paid to the possible transmission of diseases from humans to
> macaques.
>
> Problem Behaviors
>
> The most appropriate behavioral management program houses macaques in
> a sufficiently enriched and safe environment to prevent the
> development of abnormal behaviors. Nevertheless, personnel caring for
> macaques should be adequately trained and able to recognize the
> occurrence of abnormal behavior in macaques. It is important to note
> that not all macaque species exhibit the same types of abnormal
> behavior or to the same degree. Some abnormal behaviors are initially
> quite subtle in their expression, but over time can become more
> obvious and harder to stop. Abnormal behaviors include repetitive
> movements, such as pacing, circling, rocking, spinning, somersaulting
> and bouncing. Cage-licking, self-clasping, self-sucking, masturbation,
> "saluting," and eating feces are some other aberrant, repetitive
> behaviors. Abnormal behaviors in macaques also can hurt or injure the
> animals, as in the case of hair plucking, self-biting and head
> banging.
>
> Abnormal behaviors are an undesirable consequence of captive housing,
> reflecting an inadequate environment for maintaining the animal.
> Preventing the development of abnormal behaviors is critical, because
> they are difficult to stop once they start. In some cases, socially
> housing an animal that previously was singly housed can decrease the
> expression of abnormal behaviors, presuming that the animals are
> compatible. Progress has been made in reducing the occurrence of
> hair-plucking behavior by providing the animal with a fleece covered
> Plexiglas^®^ board or coconut, thereby giving the monkey something
> else to pluck. However, redirection of an abnormal behavior is not a
> "cure" and should only be regarded as a temporary correction. Although
> occasionally self-biting behavior can be redirected to a toy, recent
> evidence has shown that some drugs will reduce the occurrence of this
> behavior more reliably. In this case, the veterinarian should be
> consulted.
>
> Safety Issues
>
> In general, the least amount of restraint necessary to accomplish the
> task should
>
> be used when working with macaques. However, because macaques can
> seriously threaten people's safety, the method of restraint should
> also ensure the safety of both the personnel and the animal. Restraint
> can be achieved by hand (e.g., with younger animals), by the use of
> various drugs such as ketamine hydrochloride, or by the use of
> equipment such as transport cages, the pole and collar system, or
> tunnels to move animals from one location to another. Macaques can be
> trained to cooperate in a variety of procedures, thus reducing the
> amount of restraint necessary. Examples include training the animals
> to move into a transport box to be removed temporarily from their home
> cage or training an animal to extend its arm or leg for a blood sample
> to be withdrawn. Such training is an important part of the enrichment
> program as it gives the animal some control over the situation and
> reduces the stress the animal might otherwise experience during basic
> husbandry and medical procedures in which it was not actively
> cooperating. Appropriate protective equipment, including gloves, mask,
> eye protection, etc., should be worn when working closely with
> macaques.
>
> In addition, the provision of many types of enrichment devices involve
> either attaching the device to the cage, reaching into a cage to place
> the enrichment, or entering the primates' enclosure. These can place
> the individual at risk of being grabbed, bitten, or scratched.
> Macaques are a frequent carrier of Herpes B-virus, which is
> asymptomatic in the animals but can be fatal to humans. This viral
> infection can be transmitted from animal bites, scratches, splashes,
> needle stick injuries, and other contact with mucous membranes or
> broken skin with infected body fluids (e.g., saliva, urine) from the
> monkey. Personnel should wear appropriate protective equipment,
> concomitant with the potential for exposure.
>
> Resources
>
> National Research Council. 1998. T*he Psychological Well-Being of
> Nonhuman Primates.* Washington, DC: National Academy Press.
>
> National Research Council. 2003. *Occupational Health and Safety in
> the Care and Use of Nonhuman Primates.* Washington, DC: National
> Academy Press.
>
> Nowak R. 1999. *Walker's Primates of the World.* Baltimore, MD: The
> Johns Hopkins University Press.
>
> National Research Council. 1996. *Guide for the Care and Use of
> Laboratory Animals.* Washington, DC: National Academy Press.
>
> U.S. Department of Agriculture. 1991. *Animal Welfare Regulations.*
> Title 9, CFR Part 3, Federal Register, Volume 56, No. 32.
>
> http://www.bioserv.com (a company supplying food treats and other
> enrichments)
>
> http://www.ottoenvironmental.com/Default.asp (a company supplying
> enrichment items)
>
> http://www.enrichment.org (Web site for "The Shape of Enrichment")
>
> http://www.awionline.org/Lab_animals/biblio/enrich.htm (a bibliography
> of enrichment articles)
>
> http://www.brown.edu/Research/Primate/ (Web site for *Lab Primate
> Newsletter,* a publication with behavior and enrichment articles)
>
> http://www.aazk.org/committees/enrichment/comm_enrichment_title.php
> (Web site for the enrichment committee of the American Association of
> Zoo Keepers)
>
> http://www.aphis.usda.gov/ac/eejuly15.html (Web site for the U.S.
> Department of Agriculture's "Final Report on Environment Enhancement
> to Promote the Psychological Well-Being of Nonhuman Primates")
>
> Common Names of the Macaques
>
> *Macaca arctoides:* Stump-tailed macaque, Bear macaque, Brown
> stump-tailed macaque
>
> *M. assamensis:* Assamese macaque, Assam monkey, Mountain monkey,
> Himalayan Macaque, Montane Rhesus
>
> *M. brunnescens:* Muna-Butung monkey
>
> *M. cyclopis:* Taiwan macaque, Taiwanese macaque, Formosan macaque,
> Formosan rock macaque
>
> *M. fascicularis:* Crab-eating macaque, Cyno, Cynomolgus, Irus monkey,
> Java monkey, Kra (or Kera), Long-tail macaque, Philippine monkey
>
> *M. fuscata:* Japanese macaque, Snow monkey
>
> *M. hecki:* Heck's macaque
>
> *M. maura:* Moor macaque
>
> *M. mulatta:* Rhesus monkey
>
> *M. nemestrina:* Pig-tail macaque, Pigtail macaque, Pig-tailed
> macaque, Giant rhesus
>
> *M. nigra:* Sulawesi crested macaque, Sulawesi black ape, Celebes
> black ape, Celebes ape, Celebes crested macaque, Black ape
>
> *M. nigrescens:* Gorontalo macaque
>
> *M. ochreata:* Sulawesi booted macaque, Booted monkey, Booted macaque
>
> *M. pagensis:* Mentawai macaque
>
> *M. radiata:* Bonnet macaque, Bonnet monkey
>
> *M. silenus:* Lion-tail macaque, Liontail macaque, Lion-tailed
> macaque, Lion-maned macaque, Wanderoo, Wanderu, Ouanderu
>
> *M. sinica:* Toque macaque, Toque monkey
>
> *M. sylvanus:* Barbary ape, Barbary macaque, Gibraltar ape, Gibraltar
> macaque
>
> *M. thibetana:* Père David's stump-tailed macaque, Tibetan
> stump-tailed macaque, Tibet monkey
>
> *M. tonkeana:* Tonkean macaque
>
> Sample Pair Housing SOP \-- Macaques
>
> Pair Housing: Following are descriptions of the five different pair
> housing combinations and the procedure for pairing each combination.
> It should be noted that on-going, vigilant monitoring is necessary to
> the successful social housing program. As animals mature, their
> relationship may change, necessitating separation of the animals and
> identification of new partners.
>
> **Juveniles:** Two juveniles (three years of age or younger) of the
> same sex are paired together.
>
> *Place the animals in an appropriate size cage. Check the animals
> every hour for the first four hours and at least three times per day
> for the first week.*
>
> **Adult with Infant or Juvenile:** An adult (four years of age or
> older) of either sex is paired with a weaned infant or juvenile (eight
> months to three years) of either sex.
>
> **Adult Females:** Two adult females (generally cynomolgus monkeys,
> four years of age or older) are paired together, with their unweaned
> infants (less than one year of age), if applicable.
>
> **Adult Male and Female:** An adult male (five years of age or older)
> is paired with an adult female (four years of age or older), for
> either breeding purposes or enrichment purposes.
>
> *Place the animals in a double cage with a clear Plexiglas® panel
> between them. If there are no signs of aggression after one hour, open
> the panel. Alternatively, if a Grooming-Contact (G-C) bar divider is
> available, use this first. Check the animals at least every hour for
> the first four hours and at least three times per day for the first
> week. Initially, the animals may be separated at night, until a
> compatible relationship is established.*
>
> **Adults Males:** Two adult males (four years of age or older) are
> paired together.
>
> *Place the males in a double cage with a clear Plexiglas® panel
> between them. Alternatively, if a G-C bar divider is available, use
> this first. If there are no signs of aggression after twenty-four
> hours, move the animals to a new double cage (to avoid territorial
> aggression) without a panel. Ensure that the males do not have visual
> contact with any breeding pairs. Check the animals at least every hour
> for the first four hours and at least four times per day for the first
> week. Initially, the animals may be separated at night, until a
> compatible relationship is established.*
>
> Marmosets and Tamarins
>
> Background
>
> **Habitat**
>
> In the wild, marmosets and tamarins inhabit diverse habitats, ranging
> from Costa Rica to southern Brazil and Bolivia. They are principally
> tree-dwelling animals.
>
> **Physical Features**
>
> Marmosets and tamarins belong to the New World primate family
> Callitrichidae, which is characterized by unique morphological and
> reproductive traits. Callitrichids, among the smallest (.5 to 1.3
> lbs.) of the New World primates, often are brightly colored monkeys
> with little, if any, gender differences in body size or coloration.
> Other distinguishing morphological features of marmosets and tamarins
> include claws instead of nails on all digits except for the opposable
> hallux, and two molars on either side of each jaw.
>
> **Behavior**
>
> Marmosets and tamarins have rich communicative behavioral repertoires
> that help individuals communicate within their group and with other
> groups. Chemical communication via scent marking is one important
> aspect of callitrichid social and sexual behavior. Scent marking
> increases when marmosets and tamarins are exposed to unfamiliar
> animals. Callitrichid primates have specialized glands (found in the
> anogenital, suprapubic, sternal, and perhaps facial areas), which
> produce oily secretions that are mixed with urine and deposited on
> branches and, to a lesser degree, other surfaces. These scents contain
> information on species, subspecies, and individual identity, as well
> as reproductive status, social rank, and the age of the marking.
> Scents are also thought to facilitate reproductive suppression of
> subordinate females in some callitrichid species.
>
> **Mating and Reproduction**
>
> The social behavior of callitrichids within groups, in many ways,
> revolves around two aspects of callitrichid reproduction: reproductive
> suppression, which prevents subordinate males and females from
> engaging in sexual behavior, and extended residence of offspring in
> the natal family group. Subordinate females and adult-aged daughters
> living in their natal family group do not typically engage in
> reproductive activity and, in most cases, nonbreeding females are
> endocrinologically suppressed and do not ovulate. Likewise,
> subordinate males and adult-aged sons typically do not engage in
> sexual behavior. Reproductive suppression is known to be lifted from
> subordinate individuals when a new breeding male is introduced and
> following the death or illness of a breeding male or female.
>
> Cooperative care is another important component of callitrichid social
> life. Marmosets and tamarins typically produce fraternal twins that
> are cared for by all group members, including both male and female
> non-reproductive individuals. This is particularly important because,
> at birth, litters weigh approximately 15 -- 25 percent of adult body
> weight. Numerous studies have demonstrated that subordinate
> individuals provide a significant amount of care to infants born into
> the group. Indeed, the breeding male has been shown to participate
> less in carrying behavior when there are multiple helpers (e.g., adult
> offspring), with a concomitant increase in his survivability. The
> expression of competent caregiving behavior, however, requires
> experience with infants (either one's own or siblings). It is
> suggested, then, that individuals remain within their natal groups
> during the rearing of the next one or two litters.
>
> Social World
>
> The social lives of marmosets and tamarins are unique among primates.
> Marmosets and tamarins are the only primates known to exhibit a
> cooperative breeding system, characterized by extended residence of
> offspring within the family group, breeding that is mostly limited to
> a single breeding pair, and care of offspring provided by group
> members other than the parents.
>
> In captive settings, callitrichid primates are commonly housed in
> groups comprised of a single breeding adult male and female, along
> with the independent (subadult and juvenile) and dependent (infant)
> offspring of the breeding pair. Captive groups generally do not
> contain unrelated individuals, because social groups containing
> unrelated same-sex individuals are likely to be unstable. Studies of
> captive and wild populations of callitrichid primates, however, have
> revealed that there is some degree of intra-specific variation in
> social structure that can remain stable over long periods of time. In
> fact, a variety of different social structures have been found to
> result in stable social groups, including the following:

-   fathers with offspring

-   mothers with offspring

-   same- and opposite-sex siblings (note: opposite-sex sibling groups
    are not recommended for cotton-top tamarins)

-   same-sex pairs or small groups of unrelated or unfamiliar
    individuals

-   single same-sex or opposite-sex individuals of different species

> Intra-group aggression is generally directed toward non-breeding
> individuals by their same-sex sibling or same-sex parent.
> Displacement, threat behavior, chasing, and minor injuries often
> precede the eviction of an individual from a social group. The victim
> is easily identified because he/she will often separate from the
> group, show fearful behavior when approached by group members
> (especially an aggressor), and generally remain closer to the floor of
> the cage than other group members. Temporary separation for a period
> of hours or days may allow an individual that was in the process of
> being evicted to be reintegrated into a social group. These aggressive
> events within families are often triggered by periods of fertility in
> the dominant female, and special care should be taken to monitor group
> relations in the two to three weeks after the birth of infants, when
> the dominant females are likely to be ovulating.
>
> Introducing an adult male and female is quite easy. Generally, a brief
> period of limited contact through mesh or a "howdy cage," followed by
> a brief period of close observations once full contact is allowed, is
> all that is needed. Successfully introducing same-sex unrelated
> individuals or new adults into breeding groups, however, often is more
> difficult. In fact, the likelihood of failure increases with the age
> of the same-sex individuals already present in the group. For these
> introductions, much longer introduction and observation times are
> necessary.
>
> Physical World
>
> **Housing**
>
> An ideal captive environment for callitrichid primates promotes good
> physical health, allows for successful reproduction and rearing of
> offspring, and facilitates the acquisition of skills that the animals
> would need to survive in the wild. Although there are no clear
> specifications for optimal habitat size, habitats should be large
> enough, and rich enough, to allow and promote a full range of
> naturalistic behaviors, social interactions, and locomotion patterns.
> The general rule for callitrichid housing is that no housing is too
> large. Also, as callitrichids are tree-dwellers and range up to 10
> meters above the ground in their natural habitats, vertical space is
> extremely important. If space is limited, narrow, tall housing is
> preferred to wide, low housing.
>
> Cages often are constructed of wood or polyvinyl chloride (PVC) frames
> with steel or wire mesh. Many zoological parks also are constructing
> callitrichid housing from textured rockwork with glass or wire
> fronting. The primary furnishing for callitrichid housing should be
> natural tree branches and other surfaces on which the monkeys can
> climb, leap, and run. Branches should be arranged to provide a network
> of pathways by which the animals can move about their home. Branches
> are particularly important because marmosets and tamarins use these as
> the normal substrate for scent marking. If natural branches are not
> provided, the monkeys will scent mark on smooth, nonabsorbent
> substrates, and the marks may soil their fur.
>
> Marmoset and tamarin group members sleep huddled together, so a nest
> box, placed high in the cage should be provided. Floors should be
> covered with wood chips or shredded paper; this provides padding for
> young animals, which are most likely to fall from a branch onto the
> floor, and it also encourages animals to forage through the bedding.
> Food and water should be made available on a feeding platform or in a
> bowl placed high in the cage in a location that prevents contamination
> by urine and feces.
>
> Since wild marmosets and tamarins are highly territorial under most
> conditions, visual and auditory contact between different social
> groups should be limited. When multiple groups are housed in close
> proximity to one another, and when overcrowding occurs within social
> groups, increased aggressive behavior is not uncommon. Further,
> chronic arousal associated with prolonged exposure to unfamiliar
> animals can lead to abortions and infant loss. Visual barriers, and
> sometimes sound absorbing materials, should be used to prevent
> territorial and aggressive displays between groups.
>
> In light of the important role scent marking plays in social and
> sexual behavior, it is often suggested that husbandry practices
> maintain a sanitary, but smell-intact, environment by sanitizing cages
> less frequently and/or allowing some scent-marked items (e.g., nest
> box, perch, branches, etc.) to remain unsanitized and, thereby, retain
> their odor. However, some practical experience suggests that
> sanitizing these items routinely does not result in adverse effects on
> the health or reproductive capacity of the animals. Regardless, most
> guidelines allow for the maintenance of scent-marked branches in cages
> for periods of several weeks to several months.
>
> Environmental enrichment items and devices also are a necessary part
> of callitrichid housing. Not only do they promote the development of
> behavioral and logical skills and mental and sensory stimulation, but
> they can prompt naturally occurring behaviors in the animals. The
> amount, type, and presentation of enrichment should be varied to
> prevent boredom. Foraging devices, artificial gum trees, cardboard
> boxes and gallon milk jugs with large holes cut in them, paper towel
> and toilet paper, are commonly used for enrichment.
>
> **Feeding**
>
> Meeting the nutritional needs of callitrichid primates is essential to
> their health and well-being in captivity. The diets of wild marmosets
> and tamarins include tree exudates (sap or gum), fruits, buds and
> flowers, nectar, insects, and small vertebrates. Since proportions
> vary between and within species, only general nutritional issues will
> be covered here. However, it is important to avoid over-feeding these
> animals with food treats such that they do not consume a nutritionally
> balanced diet. Further detailed information can be found in the
> Callitrichid Husbandry Manual.
>
> Young monkeys begin to beg for and eat solid food between three to
> five weeks of age. Approximately 20 percent of the diet of wild
> marmosets and tamarins is protein. A canned marmoset diet, which is
> now commercially available, should provide the foundation of the diet.
> New World primate biscuits also should be offered, along with an
> assortment of fresh fruits and vegetables. Two fruits and two
> vegetables should be offered daily. Cooked and uncooked cereals, and
> cooked pasta, are ideal sources of carbohydrates. Treats can include
> gum arabic, marshmallows, raisins, crickets, mealworms, and waxworms.
>
> In the wild, callitrichids spend nearly 60 percent of their day
> foraging for food. Live food or highly preferred food items hidden in
> bedding simulates a natural situation and provides an additional
> opportunity for enrichment. A foraging box can be easily made by
> placing highly preferred food items into small holes that have been
> cut into a cardboard box filled with bedding. Callitrichids also enjoy
> food items suspended from branches, and treat cups with lids and peek
> holes.
>
> Special Cases
>
> **Age-related Considerations**
>
> Healthy marmosets and tamarins maintain good abilities to forage and
> move about well into their old age. The only major issue with older
> animals is difficulty in chewing solid food because of tooth wear and
> loss. In these cases, soaking food in liquids prior to feeding or
> provisioning animals with softer diets are two easy solutions.
>
> In terms of normal social development, most institutions that rear
> marmosets and tamarins have a policy of keeping young individuals in
> their family groups until they have had exposure to and experience
> with one or more sets of younger siblings. It is assumed that this
> experience will increase the likelihood of success in rearing young
> when the animals are placed in a position where breeding is possible.
> As mentioned above, however, older siblings are sometimes involved in
> mild to serious fights with same-sex siblings, and may need to be
> removed from the group. Decisions about removing an individual from a
> group should be made in light of the need for normal experience with
> siblings and the seriousness of the aggression.
>
> Rejection of infants by parents and the inability of infants to
> maintain contact with caregivers are fairly regular occurrences in
> captive marmosets and tamarins. In some cases, lack of infant success
> is associated with infant health and vigor (e.g., low birth-weight
> infants are unable to maintain a grip on their parent's fur). In other
> cases, parents (particularly mothers) may actively reject and fail to
> carry and nurse their infants. A number of zoos and research
> facilities have reported some success in hand-rearing infants.
> Specific details of hand-rearing protocols can be found in the
> Callitrichid Husbandry Manual.
>
> It is important to note that hand-rearing is associated with a variety
> of behavioral problems, particularly as the hand-reared individuals
> reach reproductive age. Therefore, decisions about hand-rearing
> rejected infants should involve a careful consideration of the
> animal's purpose in the facility as an adult. An individual that is
> highly aggressive toward people may not be a good animal for a
> zoological exhibit, for example.
>
> **Individual Housing**
>
> Like other primates, marmosets and tamarins are highly social, and
> individual or solitary housing is strongly discouraged. In the event
> that animals need to be housed individually, efforts should be taken
> to maximize regular social contact with caretakers. Marmosets and
> tamarins have been housed successfully with birds or rodents. Specific
> examples of successful mixed-species housing can be found in the
> Callitrichid Husbandry Manual. However, in no case should a marmoset
> or tamarin be housed with a New World primate from the Family Cebidae,
> including squirrel monkeys, capuchins, spider monkeys. Cebids can
> carry viruses, such as Herpesvirus saimiri, that do not affect their
> own health but could be lethal for marmosets and tamarins.
>
> In the event that animals do require individual housing, efforts
> should be taken to compensate for the isolation by providing
> additional enrichment. Increased and regular positive social contact
> with caretakers should be encouraged, but these people should be
> familiar and non-threatening to the animals. Increasing the complexity
> of the physical environment with live plants or other cage furnishings
> is also a worthwhile endeavor. Marmosets and tamarins rely extensively
> on vocalizations for communicating both within and between groups, and
> isolated animals can be stimulated to call by hearing vocalizations
> from their own or related species.
>
> Downloadable versions of vocalizations can be found in a variety of
> locations (e.g., http://pin.primate.wisc.edu/av/vocals/).
>
> Safety Issues
>
> As with all primates, marmosets and tamarins do not like handling, and
> alternatives to handling should be sought. The animals are easily
> trained to do a variety of tasks (e.g., present for physical
> examination, sit on a scale for weighing, voluntarily enter a
> transport cage). Training works best if the animals are worked
> regularly and if training occurs before the day's feeding. However,
> even well-fed animals can be trained with highly preferred food items.
> Detailed examples and descriptions of procedures can be found in the
> Callitrichid Husbandry Manual.
>
> Marmosets and tamarins should be handled as little as possible, since
> they tend to be highly reactive to unusual stressors. For routine
> procedures that are short (less than five minutes), such as physical
> examination or biological sample collection, hand-held restraint can
> work well. Animals can be captured with fine-mesh nets ("butterfly net
> mesh") and removed by hand. However, the netting procedure can be a
> major stressor for other group members. Animals can be readily trained
> to enter a detachable nest box, and removing the animal in a separate
> procedure room can minimize this distress. Handlers should wear
> protective leather gloves. A grip from behind the animal's back, with
> thumb and middle finger underneath the forearms, provides the most
> secure holding position. Most animals will take treats during this
> restraint, which can serve as a reward and enrichment during the
> handling. If handlers are also caretakers, different clothing should
> be worn during manual restraint procedures to minimize distress for
> the animals during other routine caretaking activities.
>
> For procedures of longer duration, animals should be given some form
> of chemical immobilization. Ketamine hydrochloride (intramuscular
> injection) provides good immobilization for medium-term procedures
> (5 - 15 minutes) and suggested dosages are provided in the
> Callitrichid Husbandry Manual. For long-term procedures (more than 15
> minutes) inhalable anesthetics are recommended, particularly
> isoflurane. A cat-sized face mask can be used to deliver the
> anesthetic. Some facilities have had success in inducing isoflurane
> anesthesia by placing the animal into an empty 2-liter plastic soda
> bottle with a removable bottom, and directing the anesthetic gas into
> the bottle. This procedure minimizes the struggle and stress of
> placing the mask over an awake and alert animal. For these longer
> procedures, care should be taken to monitor and maintain core body
> temperature (warming blanket or warm water bottle) since body
> temperature can drop quickly in an anesthetized animal.
>
> References
>
> Abbott DH, McNeilly AS, Lunn SF, Hulme MJ, Burden FJ. 1981. Inhibition
> of ovarian function in subordinate female marmoset monkeys
> (*Callithrix jacchus jacchus*). *Journal of Reproduction and
> Fertility* 63:335-345.
>
> Baker JV, Abbott DH, Saltzman W. 1999. Social determinants of
> reproductive failure in male common marmosets housed with their natal
> family. *Animal Behaviour* 58:501-513.
>
> Baker AJ, Savage A. 1999. Social management of callitrichids and
> *Callimico*. In *Callitrichid Husbandry Manual.* Brookfield, IL: AZA
> Neotropical TAG.
>
> Bales K, Dietz J, Baker A, Miller K, Tardiff SD. 2000. Effects of
> allocare-givers on fitness of infants and parents in callitrichid
> primates. *Folia Primatol* (Basel) 71(1-2):27-38.
>
> Byron JK, Bodri MS. 2001. Environmental enrichment for laboratory
> marmosets. *Lab Animal* 30(8):42-48.
>
> de Rosa C, Vitale A, Puopolo M. 2003. The puzzle-feeder as feeding
> enrichment for common marmosets (*Callithrix jacchus*): a pilot study.
> *Lab Animal,* 37(2):100-107.
>
> Emlen ST. 1991. Evolution of cooperative breeding in birds and
> mammals. In JR Krebs and NB Davies (Eds.), *Behavioural Ecology: An
> Evolutionary Approach* (pp. 301-335). London: Blackwell Scientific
> Publications.
>
> Epple G. 1975. Parental behavior in *Saguinus fuscicollis* ssp.
> (Callitrichidae). *Folia Primatologica* 24: 221-238.
>
> Epple G. 1986. Communication by chemical signals. In G. Mitchel and J.
> Erwin (Eds.), *Comparative Primate Biology, Volume 2, Part A;
> Behavior, Conservation, and Ecology* (pp. 531-580). New York: Alan R
> Liss.
>
> Farmerie M, Neiffer D, Vacco K. 1999. Enrichment and operant
> conditioning of callitrichids. In *Callitrichid Husbandry Manual*.
> Brookfield, IL: AZA Neotropical TAG. pp. 64-89. 
>
> French JA. 1997. Regulation of singular breeding in callitrichid
> primates. In NG Solomon and JA French (Eds.), *Cooperative breeding in
> mammals* (pp. 34-75). New York: Cambridge University Press.
>
> French JA, Inglett BJ. 1991. Responses to novel social stimuli in
> tamarins: A comparative perspective. In HO Box (Ed.), *Primate
> responses to environmental change* (pp. 275-294). London: Chapman and
> Hall.
>
> French JA, Pissinatti A, Coimbra-Filho AF. 1996. Reproduction in
> captive lion tamarins (*Leontopithecus*): Seasonality, infant
> survival, and sex ratios. *American Journal of Primatology* 39:17-33.
>
> Heymann EW, Soini P. 1999. Offspring number in pygmy marmosets,
> *Cebuella pygmaea*, in relation to group size and the number of adult
> males. *Behavioral Ecology and Sociobiology* 46:400-404.
>
> Inglett BJ, JA French, LG Simmons, KW Vires. 1989. Dynamics of
> intrafamily aggression and social reintegration in lion tamarins. *Zoo
> Biology* 8:67-78.
>
> Kinzey WG. 1997. Synopsis of New World Primates (16 Genera). In WG
> Kinzey (Ed.), *New World Primates: Ecology, Evolution, and Behavior*
> (pp. 222-296). New York: Aldine de Gruyter.
>
> Kleiman DG. 1977. Monogamy in mammals. *Quarterly Review of Biology*
> 52: 39-69.
>
> McGrew WC, Brennan JA, Russell J. 1986. An artificial "gum-tree" for
> marmosets (*Callithrix j. jacchus*). *Zoo Biology* 5: 45-50.
>
> National Research Council. 1998. *The Psychological Well-Being of
> Nonhuman Primates.* Washington, DC: National Academy Press.
>
> Poole TB. 1990. Environmental enrichment for marmosets. *Animal
> Technology* 41(2): 81-86.
>
> Rukstalis M, French JA. 2003. Exposure to conspecific vocalizations
> modulates stress responses in marmosets (*Callithrix kuhlii*).
> *American Journal of Primatology* 60 (Supplement1): 129-130.
>
> Santos CV, Martins MM. 2000. Parental care in the buffy-tufted-ear
> marmoset (*Callithrix aurita*) in wild and captive groups. *Braz J
> Biol.* 60(4):667-72.
>
> Snowdon CT, Savage A. 1989. Psychological well-being of captive
> primates: General considerations and examples from Callitrichids. In E
> Segal (Ed.), *Housing, Care, and Psychological Well-being of Captive
> and Laboratory Primates* (pp.75-88). Park Ridge, N.J.: Noyes
> Publications.
>
> Snowdon CT, Soini P. 1988. The Lion Tamarins, Genus *Leontopithecus*.
> In RA Mittermeier, AB Rylands, AF Coimbra-Filho and GAB Fonseca
> (Eds.), *Ecology and behavior of neotropical primates* (Vol. 2, pp.
> 223-298). Washington, D.C.: World Wildlife Fund.
>
> Sodaro V. 1999. Social management of callitrichids and *Callimico*.
> In *Callitrichid Husbandry Manual*. Brookfield, IL: AZA Neotropical
> TAG.
>
> Soini P. 1988. The Pygmy Marmoset, Genus *Cebuella*. In RA
> Mittermeier, AB Rylands, AF Coimbra-Filho and GAB Fonseca (Eds.),
> *Ecology and behavior of neotropical primates* (Vol. 2, pp. 79-129).
> Washington, D.C.: World Wildlife Fund.
>
> Stevenson MF, Rylands AB. 1988. The Marmosets, Genus *Callithrix*. In
> RA Mittermeier, AB Rylands, AF Coimbra-Filho and GAB Fonseca (Eds.),
> *Ecology and behavior of neotropical primates* (Vol. 2, pp. 131-222).
> Washington, D.C.: World Wildlife Fund.
>
> Tardif S, Carson RL, Gangaware BL. 1990. Infant-care behavior of
> mothers and fathers in a communal-care primate, the cotton-top tamarin
> (*Saguinus oedipus*). *American Journal of Primatology* 22: 73-85.
>
> Tardif SD, Clapp NK, Hence MA, Carson RL, Knapka JJ. 1988. Maintenance
> of cotton-top tamarins fed an experimental pelleted diet versus a
> highly diverse sweetened diet. *Laboratory Animal Science* 5: 588-591.
>
> Wissman MA. 1999. Nutrition and husbandry of callitrichids (marmosets
> and tamarins). *Veterinary Clinics of North America: Exotic Animal
> Practice* 2(1): 209-240.
>
> **Other Resources**
>
> Callitrichid Husbandry Manual, produced by the American Zoological
> Association. E-mail: bzadmin@brookfieldzoo.org
>
> *The Psychological Well-Being of Nonhuman Primates,* produced by the
> Institute for Laboratory Animal Research of the National Resource
> Council, at http://books.nap.edu/books/0309052335/html/index.html
>
> Common Names of the Callitrichids
>
> **Marmosets**:
>
> *Callithrix acariensis*: Rio Acarí marmoset
>
> *C. argentata*: Black-tailed marmoset, Silvery marmoset
>
> *C. aurita*: White-eared marmoset, Buffy tufted-ear marmoset
>
> *C. chrysoleuca*: Golden marmoset, Silky marmoset, Golden-white
> tassel-ear marmoset
>
> *C. emiliae*: Snethlage's marmoset
>
> *C. flaviceps*: Buff-headed marmoset, Buffy headed marmoset,
> White-eared marmoset, White-headed marmoset
>
> *C. geoffroyi*: White-fronted marmoset, Geoffroy's marmoset,
> Geoffroy's tufted-ear marmoset
>
> *C. humeralifer*: Santarem marmoset, Tassel-eared marmoset, Black and
> white tassel-ear marmoset, White-shouldered marmoset, Golden marmoset,
> Silky marmoset, Yellow-legged marmoset
>
> *C. intermedia*: Aripuanã marmoset
>
> *C. jacchus*: Common marmoset, White ear-tufted marmoset, Tufted-Ear
> marmoset
>
> *C. kuhlii*: Weid's black tufted-ear marmoset
>
> *C. lucippe*: Golden-white bare-ear marmoset
>
> *C. manicorensis*: Manicore marmoset
>
> *C. marcai or Callithrix argentata marcai*: Marca's marmoset
>
> *C. mauesi*: Rio Maues marmoset, Maues marmoset
>
> *C. melanura*: Black-tailed marmoset
>
> *C. nigriceps*: Black-headed marmoset
>
> *C. penicillata*: Black-eared marmoset, Black ear-tufted marmoset,
> Black-pencilled marmoset, Black-plumed marmoset
>
> *C. saterei*: Satere marmoset
>
> *Cebuella pygmaea*: Pygmy marmoset
>
> **Goeldi's Monkey**
>
> *Callimico goeldii*: Goeldi's marmoset, Goeldi's tamarin, Calimico
>
> **Tamarins**
>
> *Saguinus bicolor*: Pied tamarin, Bare-faced tamarin, Pied bare-face
> tamarin, Brazilian bare-faced tamarin
>
> *S. fuscicollis ssp*: Ávila Pires' Saddle-back tamarin, Crandall's
> Saddle-back tamarin, Cruz Lima's saddle-back tamarin, Spix's
> saddle-back tamarin, Lesson's saddle-back tamarin, Illiger's
> saddle-back tamarin, Red-mantle saddle-back tamarin, Andean
> saddle-back tamarin, White saddle-back tamarin, Geoffroy's saddle-back
> tamarin, Saddle-back tamarin, Weddell's saddle-back tamarin
>
> *S. geoffroyi*: Geoffroy's tamarin, Rufous-naped tamarin
>
> *S. graellsi*: Rio Napo tamarin, Graell's black-mantle tamarin
>
> *S. imperator ssp*: Black-chinned emperor tamarin, Bearded emperor
> tamarin
>
> *S. inustus*: Mottle-faced tamarin
>
> *S. labiatus ssp*: Red-bellied tamarin, Red-chested tamarin,
> Red-chested mustached tamarin, Thomas' mustached tamarin
>
> *S. leucopus*: White-footed tamarin, Silvery-brown bare-faced tamarin,
> Silvery-brown bare-face tamarin
>
> *S. martinsi*: Martin's tamarin, Martin's bare-face tamarin,
> Ochraceous bare-face tamarin
>
> *S. midas*: Midas tamarin, Red-handed tamarin, Golden-handed tamarin,
> Rufous-handed tamarin, Lacepede's tamarin
>
> *S. mystax ssp*: Moustached tamarin, Red-capped tamarin, White-rump
> mustached tamarin
>
> *S. niger*: Black-handed tamarin
>
> *S. nigricollis*: Spix's black mantle tamarin, Black-mantle tamarin,
> Black-mantled tamarin, Black-and-red tamarin
>
> *S. oedipus*: Cotton-top tamarin, Pinche marmoset, Cotton-head
> tamarin, Cotton-tops, Liszt monkey
>
> *S. tamarin*: Negro tamarin   
>
> *S. tripartitus*: Golden-mantled tamarin, Golden-mantle saddle-back
> tamarin
>
> *S. weddelli*: Weddell's tamarin
>
> Squirrel Monkeys
>
> Background
>
> **Habitat**
>
> Squirrel monkeys are inquisitive, predominately tree-dwelling primates
> that spend the majority of their time in the middle level canopy of
> the forest. Their distribution includes an isolated population in the
> rainforest of Costa Rica and virtually the entire Amazon Basin of
> South America. In the wild, squirrel monkeys inhabit most types of
> tropical forest including both wet and dry forest, continuous and
> secondary forest, mangrove swamps, riparian habitat, and forest
> fragments. They are very flexible in their ability to adapt to
> different environments and, in some geographic areas, appear to prefer
> habitats that have been disturbed by humans.
>
> **Physical Features**
>
> The male squirrel monkey weighs approximately 550-1135 grams, while
> the female weighs from 365-750 grams. The male exhibits an increase in
> body weight\-- particularly in the arms, shoulders and trunk of the
> body\-- during the breeding season, referred to as the "fatted male"
> syndrome. This increase in body weight is accompanied by an increase
> in spermatogenesis. The tail of the squirrel monkey is long, but not
> prehensile. The legs are longer than the arms. The hair coat is short
> and dense, with coloring ranging from grey-green on the back of the
> animal to white, yellow or orange on the underside. There is typically
> a tuft of black hair on the tip of the tail.
>
> **Behavior**
>
> Squirrel monkeys are omnivores that eat insects, eggs, and small
> vertebrate animals, in addition to various fruits, flowers, and tender
> leaves. In captivity, squirrel monkeys can live to be 25 years of age.
>
> Squirrel monkeys primarily use all four limbs to move, employing their
> tails for balance as they navigate along tree branches. They
> occasionally stand on two limbs to walk short distances and to grasp
> food items with both hands. As a tree-dwelling species, they make use
> of vertical as well as horizontal space. Although they often descend
> to the ground or floor of their enclosure, they prefer to leap from
> perch to perch. Lacking the bone structure for sitting, they perch
> rather than sit, frequently using their tails for balance. Perches
> should be round in shape rather than flat shelves, as the development
> of pressure sores on the tail has been associated with flat shelves.
>
> Social interactions frequently observed within squirrel monkey groups
> include grooming behaviors, "calling" (i.e., vocalizations), play,
> displays of aggression, and huddling. Vocalizations help to maintain
> the social organization of squirrel monkey troops. Squirrel monkeys
> use calls to enhance group coordination and cohesion. It has been
> suggested that squirrel monkeys can differentiate individuals using
> vocal cues and communicate within the troop even when they cannot see
> each other.
>
> Communication between animals within a given social group includes
> olfactory, visual, and vocal signals. Olfaction is most important
> during the breeding and birthing seasons. Males use scent to determine
> the receptivity to mating of females. In addition, female monkeys use
> scent to identify individual infant animals. When cleaning the
> animals' enclosures, it is beneficial to the monkeys to avoid strong,
> artificially scented products.
>
> Visual cues are of primary importance in visual displays. Squirrel
> monkeys make these displays in an attempt to assert dominance or
> reduce tension between individuals. Visual cues involving facial
> expressions can be associated with fear or aggression. A penile
> display, associated with spreading of the thighs, is considered to be
> a dominance gesture. Enclosures should provide a place for a
> submissive monkey to break the stare of a more aggressive monkey. Such
> places are called "hide-boxes" and can be made from a piece of a
> large-diameter polyvinyl chloride (PVC) pipe or another impervious
> material.
>
> Vocal signals are of the utmost importance for squirrel monkeys.
> Infants possess a wide repertoire of sounds, including grumbles,
> cackling, purrs, chucks and peeps. These sounds communicate the
> well-being of the infant to the mother. In adults, calls are used to
> signal alarm, to display general disturbance or excitement, and to
> establish contact with the group when visually separated.
>
> **Mating and Reproduction**
>
> Social behavior in squirrel monkeys depends on the phase of the
> reproductive cycle. These monkeys become sexually mature at
> approximately three to four years of age. While reproductive
> efficiency declines beginning at about 12 years of age, they can
> continue to reproduce for several more years. During breeding season
> (December through February in the northern hemisphere), male monkeys
> tend to be more inquisitive, aggressive, and active. At the same time,
> receptive female monkeys are less likely to respond with an aggressive
> display or facial expression when approached. After the breeding
> season, males become less involved in the social group, often
> remaining on the perimeter of the group. Females tend to perch with
> other females of similar age. These female-female interactions may
> include infant-care sharing and grooming behaviors.
>
> The gestation period lasts approximately 168-182 days. During the
> birthing season (usually May to August in the northern hemisphere),
> older females without infants will act as "baby-sitters" or "aunts,"
> often carrying infants for the mother. This maternal behavior by
> females other than the mother may include nursing another female's
> infant. This is a common characteristic of squirrel monkey breeding
> groups. Occasionally, juvenile animals can pose a threat to nursing
> infants as they can be aggressive to the new babies. Care should be
> taken when housing expectant/new mothers with juvenile animals.
>
> Social World
>
> Consideration of the needs of squirrel monkeys in captivity should
> extend beyond their basic physiologic requirements. These animals
> possess a host of behaviors that define their species. Putting forth
> the effort to enhance psychological and physical well-being of
> squirrel monkeys is essential to meeting the needs of this species.
> Through a well-conceived plan of environmental enrichment, good
> husbandry practices and a sound program of veterinary medical care,
> anxiety and boredom can be alleviated and natural behavior typical of
> this species can be promoted.
>
> In the wild, squirrel monkeys live in large social groups ("troops")
> containing 20 to 200 animals. In captivity, social group size and age
> and sex ratios differ depending on the limitations of the housing
> available and purpose for maintaining the animals.
>
> Efforts should be made to house the highly social squirrel monkeys in
> pairs or small groups whenever possible. Social groups should be
> maintained with animals born into the social group remaining in the
> group as long as is possible. Generally, it is recommended that social
> groups maintained in captivity include only one or two adult males per
> group, because fighting may develop among males if more than two are
> housed together within the social group. Most of the time, females of
> varying ages can be housed in social groups of two or more with only
> occasional difficulties with incompatibilities of group members. In
> fact, housing multiple females per group provides breeding animals the
> social structure necessary to reproduce efficiently. To maximize
> breeding efficiency, as many as 20 females can be housed with a single
> male. An optimal ratio, however, is one male per eight to ten females.
>
> Groups that have access to a semi-natural environment with more living
> space are able to accommodate more adult males within the same
> groupings due to the increased complexity and size of the environment,
> the possibility of emigration to an adjacent group within the
> enclosure, and the increased provision of hiding areas.
>
> Physical World
>
> **Housing**
>
> Both indoor and outdoor group pens can be designed for squirrel
> monkeys. Physical comfort of the animals is important in reducing
> stress and promoting the well-being of colony members. Animals in
> outdoor pens have the opportunity to control aspects of their
> environment by moving through their pen (e.g., sun or shade). The
> animals are generally free to seek the place they wish to spend their
> time. Animals in these pens can also self-regulate the amount of
> exposure to other animals by moving within their pen. Perches should
> be positioned at several levels within the living area for climbing
> and jumping. These perches can be constructed of PVC pipe, which is
> impervious to water, easily cleaned and not highly thermoconductive.
> Wood perches can also be used as long as they are replaced once they
> become excessively soiled or become otherwise deteriorated. As noted
> previously, flat shelves should be avoided due to the potential
> development of pressure sores on the tail of the animal. Large PVC
> pipe sections can be provided for animals to "hide" in, allowing them
> to break eye contact with other members of their social group during
> aggressive encounters. Finally, certain positions within the pen allow
> the monkeys to view, and be viewed by, other social groups, while
> other positions will greatly restrict the number of other animals the
> individual can see or be seen by.
>
> Animals housed in indoor cages, on the other hand, have a limited
> ability to regulate their exposure to animals housed in other cages by
> positioning themselves in such a way as to limit their ability to view
> other animals. Cage configuration will determine the number of monkeys
> that can be housed. Rack caging can be used to house small groups,
> pairs, or single animals. These cages should also have perches at
> varying heights to enable the animals to maximize their
> three-dimensional use of space. The *Guide for Care and Use of
> Laboratory Animals* (NRC 1996) and the Animal Welfare Regulations
> (1991) provide minimum cage space guidelines and requirements.
>
> In the laboratory setting, it is best to allow the animals to
> communicate through olfactory, visual, and vocal signals. Even in
> singly-housed animals, this communication can be preserved by
> arranging the cages to enable the animals to smell, see, and hear each
> other. Outside noise should be kept to a minimum so that the
> group-housed monkeys can hear each other's vocalizations. By
> group-housing animals whenever possible, communication becomes an
> important form of social enrichment.
>
> Each cage should be provided with swings, moving perches, or objects
> hanging within the cage. These can be made of either a plastic chain,
> looped PVC tube, or other similar materials. Smaller, rack-mounted
> cages will need to have at least one such device, while larger group
> cages should have two or more, depending on the number of monkeys in
> the cage. Loose hanging devices should not be included in individual
> cages where the room taken up by the swing would limit movement of the
> animal or where the swing is not appropriate for clinical reasons.
>
> Being neotropical primates, squirrel monkeys thrive in warm
> temperatures. In captivity, temperatures should be maintained between
> 78°-85°F. Relative humidity should be maintained above 50% if
> possible. If relative humidity falls below 30%, squirrel monkeys can
> develop crusts around the nostrils and frequent sneezing. Special care
> must be taken in cooler climates to prevent hypothermia.
>
> **Enrichment**
>
> In all caging conditions, a number of different food items and perch
> arrangements can be used to vary the environment of the animals and
> consequently increase activity levels and sensory stimulation. Perch
> arrangements with hanging objects, such as infant toys and practice
> golf balls, should be rotated and replaced routinely. Objects must be
> large enough to prevent swallowing and sturdy enough not to be broken
> into small pieces. Food treats should be nutritious. Fruit and
> vegetables must be selected for quality and should be washed prior to
> feeding.
>
> Occasionally, squirrel monkeys can experience anxiety when exposed to
> novel stimuli. Care must be taken, particularly with animals in
> smaller enclosures, to ensure that changes are not distressing to the
> animals. Animals should be observed after introduction of new objects
> to determine whether they show signs of fear or avoidance of the
> object. If this occurs, the object should be removed. In larger
> enclosures, this is less of an issue, as the monkeys can move away
> from new objects and acclimate slowly.
>
> **Feeding**
>
> The animal's primary diet should be an appropriate, commercially
> available diet. In addition, each monkey's diet should be supplemented
> with fruit and vegetables according to what is seasonally available
> (although squirrel monkeys can have problems with their teeth
> associated with a high sugar diet; therefore, vegetables are preferred
> over sweet fruits). Items may include melon, oranges, apples (note
> that there is some evidence that apples may be associated with bloat,
> a frequently fatal disease where the stomach fills with gas), Kiwi
> fruit, strawberries, pears, bananas, grapes, celery, bell peppers,
> tomatoes, carrots, and sweet potatoes. Additional items, such as
> various flavors of Gatorade^®^, multi-vitamins, and food-pellet
> rewards for correct responses may be added for experimental or
> clinical reasons. To encourage foraging, food items can be placed in
> the cage or pen floor after daily cleaning. This encourages the
> animals to move about the cage to select their food. Additional food
> items can be placed in hanging PVC tubes that require the monkeys
> reach into the tube to find food items.
>
> Highly desired food items should be handed out by caregivers at least
> twice daily, for example during daily observations of the animals.
> This positive interaction with caregivers allows the animals to
> habituate to the caregivers and allows the caregivers to interact in a
> non-threatening, positive way with the animals.
>
> **Sanitation**
>
> Standards for the sanitation of caging for squirrel monkeys housed
> indoors are well-described in the National Research Council's *Guide
> for the Care and Use of Laboratory Animals* (1996). However, many
> squirrel monkeys are housed in semi-naturalistic environments, where
> they may be exposed to numerous parasite hosts, such as mollusks,
> frogs, and small snakes as well as soil and water that may have been
> contaminated by rodents carrying transmissible diseases such as
> leptospirosis. Sanitation programs should include diligent exclusion
> of slugs, snails, frogs, rodents, and as many insects as
> possible---particularly in tropical environments---to minimize
> exposure of the animals to these parasite and disease hosts.
>
> Special Cases
>
> **Age-related Considerations**
>
> If possible, infants and young juveniles should be housed with their
> mothers and remain within their natal social group. Attempts should be
> made to find appropriate foster-mothers for newborn infants that are
> rejected or orphaned. Failing this, or if the newborn is clinically
> compromised and unable to cling normally to a female, it can be housed
> in a separate nursery. Nursery infants can be housed in small,
> wire-mesh cages. They should be given a cloth surrogate mother
> approximately the same diameter as an adult female monkey to provide
> contact comfort. Infants in the nursery need frequent, positive
> contact from the caregivers as part of the feeding schedule. This
> contact varies from every hour to every four hours depending upon the
> age of the animal. As the infants grow older and strong enough to
> interact with other infants, they can be moved to a larger enclosure
> with other similarly aged infants. The cage should be equipped with
> multiple levels of perching and swings for the animals to move and
> jump from one to the next. When nursery-reared infants become old
> enough (6 - 12 months of age) to eat on their own and move about
> within a social group with adults, they can be introduced into a
> social group within the general colony.
>
> **Individual Housing**
>
> Abnormal social behavior (e.g., over- or under-aggressiveness) that is
> the result of incompatible social partners can result in an individual
> being removed from its current social group to another social group or
> individual housing for a\
> period of time. If the animal is a danger to other animals, a
> qualified veterinarian should determine whether the animal should be
> placed in an individual cage. In addition, individual housing should
> be considered when animals cannot defend themselves from the normal
> dominance-related aggression that occurs in this species and for acute
> or chronically sick and debilitated animals.
>
> All individually housed animals should be provided with multiple
> perches, varied foods, and frequent contact with familiar caregivers.
> The U.S. Department of Agriculture requires that exemptions (e.g., for
> health or behavioral reasons) from social housing must be recorded by
> the attending veterinarian. In research programs, the Institutional
> Animal Care and Use Committee may exempt individual animals from
> participating in the social enrichment portion of the enrichment
> program when such housing is justified for experimental reasons. Every
> attempt should be made to ensure that there is direct visual,
> auditory, and/or olfactory contact with other squirrel monkeys.
> Animals that are unable to see and hear other squirrel monkeys may be
> given access to auditory stimuli from another room containing squirrel
> monkeys via a microphone-speaker arrangement or a pre-recorded audio
> tape. Extra contact with familiar caregivers should be provided. In
> addition to frequent visits, caregivers should provide much-desired
> food treats. Live prey, such as mealworms and crickets, can be used to
> increase the stimuli that food treats can provide. Toys, perches,
> swings, and other hanging devices should be rotated more frequently.
> Mirrors can also be used to provide sensory stimulation.
>
> Attempts to socially house squirrel monkeys should be documented for
> both internal tracking purposes and for government regulatory
> agencies. Some animals that do poorly in large social groups can be
> housed together with a small number of other animals that similarly
> can not live in large social groups. This arrangement will allow
> social contact with other squirrel monkeys while reducing the level of
> competition for resources.
>
> Problem Behaviors
>
> Abnormal non-social behavior, including stereotypical movements and
> self-injurious behaviors, may necessitate a change in housing
> structures, enrichment objects or reinforcement techniques. For
> example, "pacing" may be eliminated by increasing the animal's
> available travel paths by installing additional perches. Self
> injurious behavior, such as self hair-pulling and self-biting, often
> are the result of unusual stress. If such behavior is seen in an
> animal, an evaluation should be made of the animal's current social
> status and housing environment. These animals should also receive a
> physical examination by a veterinarian to determine their health
> status.
>
> Safety Issues
>
> By far the most effective method for restraining squirrel monkeys is
> the use of leather gloves designed for handling small primates. These
> gloves provide protection to the human worker while preventing injury
> to the monkey. As with any restraint technique, technicians must be
> adequately trained to assure that the animal is restrained without
> injuring it. With practice and continued vigilance, the use of heavy
> leather gloves is a safe method of restraint for both the handler and
> the monkey. The use of nets to catch/restrain squirrel monkeys is not
> recommended. These animals are prone to fractures of the appendages
> when nets are used.
>
> Squirrel monkeys can be trained to jump from cage to cage during rack
> changes. For cleaning of larger enclosures, it is not necessary to
> remove the animals prior to cleaning as long as noxious chemicals are
> not used and if the animals can perch above or away from the area
> being cleaned.
>
> Chemical restraint may be considered by the veterinarian to restrain
> squirrel monkeys for transport and medical care in an attempt to
> reduce the stress and hazards associated with working with these
> monkeys. Ketamine hydrochloride, either with or without xylazine, can
> be used by the veterinarian for brief sedation.
>
> Squirrel monkeys are wild animals and must be treated as such. They
> can injure caregivers through bites and scratches. But because they do
> not carry *Cercopithecine herpesvirus 1* (*Herpesvirus simiae* or
> B-virus), a bite or a scratch from a squirrel monkey can be treated
> much like the bite from a domestic dog or cat. Regardless, care must
> be taken when handling these animals to prevent injury to both the
> caregiver and the animal.
>
> While it is unlikely that infectious diseases would transfer from
> squirrel monkeys to humans, and vice versa, common-sense precautions
> should be taken when working with any animal: immunocompromised
> workers should not handle animals with any known illness; masks should
> be worn when aerosols are present; any worker with an active upper
> respiratory infection should not handle animals; and consultation with
> a health professional may be necessary. Finally, although current
> human vaccination protocols include vaccination against measles,
> should an infection occur in any individual who resides with the
> animal caregiver, that caregiver should avoid any contact with
> squirrel monkeys until the infection has resolved. Measles spreads
> rapidly and is fatal in squirrel monkeys.
>
> References
>
> Abee CR. 1985. Medical care and management of the squirrel monkey. In
> LA Rosenblum and CL Coe, eds., *Handbook of squirrel monkey research,*
> 447-488. Plenum Press: New York.
>
> Abee CR. 2000. Squirrel monkey (*Saimiri spp.*) research and
> resources. *ILAR Journal* 41:2-9.
>
> Brady AG. 2000. Research techniques for the squirrel monkey (*Saimiri
> sp.*). *ILAR Journal* 41:10-18.
>
> DuMond FV. 1968. The squirrel monkey in a seminatural environment. In
> L.A. Rosenblum and R.W. Cooper, eds. *The Squirrel Monkey,* 31-68. New
> York: Academic Press.
>
> Dunn FL. 1968. The parasites of *Saimiri*. In L.A. Rosenblum and R.W.
> Cooper, eds. *The Squirrel Monkey,* 31-68. New York: Academic Press.
>
> Napier JR and Napier PH. 1967. *A Handbook of Living Primates.* New
> York: Academic Press.
>
> National Research Council. 1998. *The Psychological Well-Being of
> Nonhuman Primates.* Washington, DC: National Academy Press.
>
> National Research Council. 1996. *Guide for the Care and Use of
> Laboratory Animals.* Washington, D.C: National Academy Press.
>
> Reinhart V (ed). 1997. *Comfortable Quarters for Laboratory Animals,
> 8th edition.* Washington, DC: Animal Welfare Institute.
>
> Rosenblum LA, Coe CL (eds). 1985. *Handbook of Squirrel Monkey
> Research.* New York: Plenum Press.
>
> United States Department of Agriculture, Animal and Plant Health
> Inspection Service. 1999. *Final Report on Environmental Enhancement
> to Promote the Psychological Well-Being of Nonhuman Primates.*
>
> Williams LE, Abee CR, Barnes SR, Ricker RB. 1988. "Cage design and
> configuration for an arboreal species of primate." *Laboratory Animal
> Science.\
> *38: 289-291.
>
> Common Names of Squirrel Monkeys
>
> *Saimiri boliviensis:* Bolivian squirrel monkey, Peruvian squirrel
> monkey
>
> *S. oerstedii:* Grey-crowned Central American squirrel monkey,
> Black-crowned Central American squirrel monkey
>
> *S. sciureus:* Humboldt's squirrel monkey, Ecuadorian squirrel monkey,
> Common squirrel monkey, South American squirrel monkey
>
> *S. ustus:* Bare-eared squirrel monkey, Golden-backed squirrel monkey
>
> *S. vanzolinii:* Blackish squirrel monkey, Black squirrel monkey,
> Black-crowned squirrel monkey, Black-headed squirrel monkey