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In: Laboratory Animal Medicine and Management, Reuter J.D. and Suckow M.A. (Eds.).

International Veterinary Information Service, Ithaca NY (www.ivis.org), Last updated: 27-Mar-2006;


B2507.0306
Biology and Medicine of Non-human Primates. Part I: Physiology and
Management
M.J. Linn 1 , R. Duran-Struuck 2 , A.K. Trivedi 3 , L.B. Zajic 4 , S.K. Wrobleski 5 , A.E. Hawley 6 and D. D. Myers Jr. 7
2,7 Unit for Laboratory Animal Medicine and 1,3,4,5,6,7 Jobst Vascular Laboratory, Section of Vascular Surgery, Department

of Surgery, University of Michigan Medical Center, Ann Arbor, MI, USA.

Table of Contents
Introduction
Basic Biological Normative Data
Anatomy
Nutritive Requirements
Normative Hematology
Husbandry and Management
Environmental Enrichment
Primate Reuse and Retirement
Management
Occupational Health and Safety
Primate Resources
References

Introduction
Nonhuman primates represent a diverse population of mammals that are taxonomically similar to humans. These
similarities to humans in anatomical and physiological functions have made the evaluation of nonhuman primates an
integral part to advancement of biomedical research. The purpose of this book chapter is to provide an overview of the
primary nonhuman primate species evaluated and utilized in the biomedical research community. In this chapter, we have
also provided references that will facilitate the comprehensive study of selected areas of interest.

Biology
Basic Biological Normative Data
Taxonomy
The order Primates is broken into three suborders, Prosimii, Tarsioidea, and Anthropoidea. The Anthropoidea suborder
includes the Platyrrhini (New World monkeys) and the Catarrhini (Old World monkeys), enveloping a broad variety of
monkey species. Tarsioidea belong to a recently recognized suborder of Primates, and they are believed to fall into the
evolutionary middle ground between the Anthropoidea and Prosimii. The Prosimii (or prosimians) are generally considered
to be "pre-primates", possessing more primitive characteristics when compared with the other suborders previously
mentioned [1].

Distinctive Features of Infraorders


Prosimian Lemuriformes have cat-like faces with a fissured upper lip and a moist, hairless snout (rhinarium), and are not
considered to be monkeys. Lemuriformes have a toothcomb (lower incisors and canines) and a "toilet claw" to assist in
grooming. They are indigenous to Southeast Asia, India, and Africa, and all have epitheliochorial placentas [2].
Lemuriformes are not traditionally used in research, so they will not be discussed extensively.

Tarsioidea were considered Prosimians until just recently, when they became their own suborder. They share some
characteristics with Prosimians, and some with Anthropoidea. Tarsioidea are nocturnal, like most Prosimians; and have
hemochorial placentas like Anthropoidea [2]. They also are not traditionally used in research.
Platyrrhine, or New World monkeys (NWM), are arboreal primates indigenous to Central and South America. They
possess flattened muzzles with round, widely-spaced nostrils, and some have prehensile tails. The Callitrichidae family,
including marmosets and tamarins, has sharp claws, unlike the rest of the primates, who possess long, curved nails. Unlike
Old World monkeys (OWM), NWM do not possess ischial callosities or cheek pouches. All Platyrrhine are diurnal, except
Aotus, and have hemochorial placentas. Cebus menstruate, but all other Platyrrhine have estrous cycles. New World
monkeys are unable to convert vitamin D 2 , so they require vitamin D 3 in their diet. Callitrichidae (marmosets and
tamarins), Aotus (owl monkeys) and Saimiri (squirrel monkeys) are the New World monkeys that are regularly used in
biomedical research.

Catarrhine (Old World) monkeys are indigenous to the extreme southern end of Europe, Asia, and Africa and are the
primates most similar to humans. One of their distinguishing features is the elongated muzzle with closely spaced comma-
shaped nares. Some OWM have cheek pouches, and some have ischial callosities for protection when sitting, and many
have sex skin that swells around the time of ovulation. They do not possess prehensile tails, despite some species being
mainly arboreal. All OWM are diurnal, have hemochorial placentas, and are able to metabolize vitamin D 2 into vitamin
D 3 . Old World monkeys that are most often used in biomedical research are Macaca mulatta (rhesus monkeys), Macaca
fascicularis (cynomolgus monkeys), Papio species (baboons), and Pan troglodytes (chimpanzees).

Biological Data of Callitrichidae


Callithrix jacchus jacchus (common or tufted marmoset) is the species in this family most widely used for research. Abbott
et al. has recently published a complete overview on the basic biology and life history of the common marmoset used in
biomedical research [3]. Adult male marmosets weigh 225 to 493 grams (g); while adult females weigh 182 to 387 g [1,4].
Two tamarin species are regularly used in laboratory research: Saguinus oedipus oedipus (cotton-top tamarin) weigh 425 to
550 g, and S. mystax (mustached tamarin) weigh 600 to 650 g, with very little sexual dimorphism in either [1,5].
Callitrichidae are diurnal monkeys that typically eat insects, fruits, and vegetables in the wild, but are fed fruit and chow in
the laboratory setting. Most possess non-prehensile tails, long legs, non-opposable thumbs and, except for a flat nail on
their big toes, have claws [6-8]. All Callitrichidae possess 32 teeth with the formula 2.1.3.2 / 2.1.3.2 [6].

The estrus cycle of C. jacchus is approximately 28.6 days, with the follicular cycle lasting eight and a half days, and the
luteal phase lasing 19 to 21 days [2]. Estrus occurs mid-cycle, wherein sexual activity increases, and marmosets do not
menstruate [5]. The estrous cycle can reportedly be monitored by detecting changes in hormone levels in urine, feces, or
the blood [2].

Callitrichidae social groups vary in make-up; typically there are two to 15 members, with the highest ranking male and
female being the only breeding pair [2,4]. Groups can be one female-multi-male, one male-multi-female, or multifemale -
multimale, and tend to include several offspring and a couple immigrant animals. Cycling in non-dominant female
marmosets and tamarins in a group is often non-existent due to scent marking by the dominant female, although cycling
will occur within a matter of days when a non-dominant female is moved into a pairing with an unrelated male. Twinning
is extremely common in both marmosets and tamarins in the wild (C. jacchus, 80%), and it has recently been documented
that triplets are the most commonly produced litter size among established captive -reared colonies [2]. Tardif et al. has
recently published a complete overview on the reproductive biology of the common marmoset in captivity [9]. Callithrix
are capable of pregnancy within two to four weeks of giving birth, and are assisted by males and other offspring during the
six month weaning process. These other caretakers play a prominent role in carrying the young offspring and providing it
with solid food [10]. With a 145 day gestation, it is common for Callithrix mothers to have two pregnancies per year [5].
Mating occurs year-round. Saguinus have a gestational period of 140 days, with up to 100 g of weight gain during
pregnancy [6]. Twinning is common in the wild, but singletons are the norm in captivity among Saguinus.

Biological Data of Aotus


Aotus (Owl monkeys) are the only nocturnal New World primate genus, and adults weigh approximately one kilogram,
with very little sexual dimorphism (Fig. 1 ) [11]. These quadrupeds have long hind limbs, which allow them to leap from
tree to tree in the forest, using their claws to cling to the bark of trees [12]. Cebidae (Aotus and Saimiri) possess 36 teeth
with the formula 2.1.3.3 / 2.1.3.3 [8].

Figure 1. Aotus tivirgatus (Owl monkey) [ 11]. - To view this image in full size go to the IVIS website
at www.ivis.org . -

Owl monkeys use a number of means of communication. They will urinate on their hands and then rub their hands on
branches and other items in order to communicate sexual attraction. They also smell each other when first meeting and
before mating. Aotus sp. are very vocal communicators, making sounds ranging from squeaks and high trills that allow
infants to locate their mothers, to screams that permit adults to warn group members of impending peril. Owl monkey
species show aggression by arching their backs, either from a quadrupedal or bipedal stance, and they discourage predators
from attacking by rapidly swaying back and forth, making it clear to the predator that the monkey is aware of its presence
[12 ].

The typical owl monkey group consists of a monogamous breeding pair and their offspring, which remain with the group
until they reach two and a half to three and a half years of age, at which time they disperse to find their own mates [12].
The father takes on the caregiver role, and in the event of his death, other offspring, not the mother, will assume his role.

Social grooming only occurs before and after copulation attempts, regardless of their success, and it involves the use of one
animal’s hands and teeth to remove dead skin, hair, and insects from the coat of its partner animal. Mating occurs after the
pair sniffs each other, in the dorso-ventral position, and ejaculation takes place after three to four pelvic thrusts [12].
Gestation in Aotus is 133 days, and this genus needs to be karyotyped before breeding, due to variability in chromosome
number and homology among the taxa [5,13 ].

Biological Data of Saimiri


Adult male Saimiri sciureus (common squirrel monkey) weigh 700 to 1100 g, while females weigh 500 to 750 g [14 ].
Squirrel monkeys display some sexual dimorphism; males tend to dominate in weight and body length, while females tend
to possess longer tails (Fig. 2 ) [6,11]. Male S. sciureus also have longer canine teeth than females. Their legs are longer
than their arms, allowing for occasional bipedalism, and they sometimes use their non-prehensile tails as anchors when
standing upright. In infants, the black -tipped tails are prehensile, but they lose this ability as the monkeys grow into
adulthood. Squirrel monkeys have pseudo-opposable thumbs and have demonstrated impressive tactile sensitivity [5,14 ].

Figure 2. Saimiri sciureus (common squirrel monkey) [11]. - To view this image in full size go to the
IVIS website at www.ivis.org . -

Squirrel monkeys have been known to live in groups of over 500 individuals in the wild, but are subdivided into bands of
adult males, mothers and infants, and juvenile bands, which rejoin during mating season [5,6]. Male dominance is shown in
an elaborate penis display, rather than the mounting display preferred by Old World monkeys. Mutual grooming is rare and
is not associated with sexual behavior. Infants cling to the back of their mothers unaided and crawl to her chest to nurse.
They continue to cling even when sleeping. Gestation is 168 - 182 days, and twinning is rare [6]. Males reach sexual
maturity at four years, and females at two and a half years of age [5]. Life expectancy in captivity is approximately 20
years [5].

Biological Data of Macaca


Macaca mulatta (rhesus macaque) and Macaca fascicularis (cynomolgus, long tail, or crab-eating macaque) are the
members of the Macaca genera most commonly used in research (Fig. 3) [11]. Both species are diurnal and sexually
dimorphic and have pouches in their cheeks in which they can store food while they forage. Adult females weigh three to
four kilograms, and males of both species weigh about six kilograms [15,16]. Macaques possess ischial callosities, which
are hardened, hairless pads that are fused to the ischial bones. In males, these are fused at the midline, and in females they
are two separate pieces, separated by the genitalia [17]. Macaques use vocal signals, coos, and barks to signal each other
and their handlers, but they tend to be particularly expressive in their use of body language and facial expressions. They
will retract their lips while clenching their teeth together in a display meant to reduce aggression in tense encounters.
Additionally, maintaining eye contact (staring) is a threatening behavior, and a macaque will stare while holding his mouth
open, but covering his teeth with his lips. Males are known to smack their lips as an invitation to a female in estrous to
copulate [15,16].

Figure 3. Macaca mulatta (Juvenile rhesus macaque) [11]. - To view this image in full size go to the
IVIS website at www.ivis.org . -

Both species have multimale -multifemale social systems and are promiscuous, but in cynomolgus societies, the alpha male
dominates the sexual activities. Sex skin, which can involve swelling and engorgement of the vulva, thighs, perineal region
and hairless areas of the chest neck and face is more active in younger rhesus females than in more mature females, and
both genders normally have reddish buttocks. Male M. mulatta also experience further reddening of the buttocks and back
of the legs during mating season when in the presence of menstruating females [16 ]. Females reach sexual maturity by
three and a half years and males by four years, but males contribute little as breeders in their first few years of sexual
maturity [1]. Full growth is attained at six and ten years, respectively [5]. The rhesus has a gestational duration of 165 to
178 days, with a mean birth weight of 475 g, while M. fascicularis has a slightly shorter gestation of 155 to 165 days and a
mean birth weight of 345 g [1,8].

Biological Data of Papio


Baboons are diurnal nonhuman primates with a wide range of habitats and food sources, with species ranging over the
continent of Africa and throughout the Middle East. All species of Papio exhibit varying degrees of sexual dimorphism.
The male olive baboon (P. anubis) weighs around 25 kg, while the females weigh about 14 kg [18] (Fig. 4) [ 11].
Hamadryas baboons (P. hamadryas) weigh between 20 and 30 kg for males, and around ten to 20 kg for females [19].
Baboon hair occurs in a range of shades from olive-gray to an orangey-brown, and the males of some species have manes
of long hair surrounding their faces. Like macaques, baboons have ischial callosities fused to their ischial bones, which are
connected at the midline in males, and are separated into two pieces by the genitalia in females. In the wild, hamadryas
typically live in groups consisting of single males with harems of females that gather with other groups at night to sleep on
rocky outcroppings, while P. anubis live in promiscuous multimale -multifemale groups [18].

Figure 4. Papio anubis (Adult male olive baboon) [11 ] - To view this image in full size go to the IVIS
website at www.ivis.org . -

Baboons communicate with each other and their handlers both vocally and by physical means. Papio anubis, males in
particular, are capable of a number of bark-like vocalizations. Their vocalizations can convey aggression among animals,
toward handlers, or as warning to the other animals. Captive baboons show aggression toward their human handlers with
expressions similar to those they use toward other animals: they will yawn widely, revealing their sharp canine teeth, which
is often done while raising the eyebrows and scalp, revealing a contrasting lighter shade on their eyelids. An adult male will
sit with his erect penis in view, as a reminder to others of his presence. Baboons also will "present" their back ends in a
submissive posture when threatened [18]. The menstrual cycle of P. anubis lasts 30 - 37 days, with menstruation lasting
from one to six days [1]. In female P. anubis, sexual maturity is reached in three to four years, and 3.5 to 4.5 years in males
[1]. The perineum of P. anubis turns a bright red during pregnancy. The gestational period for the olive baboon is 173 to
193 days, with a mean birth weight of 865 g. Infants are weaned between six and 15 months of age, but the olive baboon ’s
inter-birth interval is 18 to 24 months, allowing time for the offspring to learn from its family group [1]. Infanticide has
been observed in the olive baboon [18 ]. The life span for baboons is 30 to 40 years [5].

Biological Data of Pan


The common chimpanzee (Pan troglodytes) exhibits sexual dimorphism; the males weigh about 40 kg, while the females
weigh 30 kg. At around 85 cm in length, males are about 8 cm taller than females [5]. Chimpanzees have light or mottled
skin with black hair and no tail or ischial callosities; infants and youth have tufts of white fur on the anal area (Fig. 5) [11 ].
These apes use the knuckles of their hands for quadrupedal motion, but are capable of bent-knee bipedalism and many of
the tree-top acrobatic activities of monkeys. Chimpanzees have long fingers, and a short fully opposable thumb, which
prevents them from performing a precision grip, much like humans use to hold a pencil. They are capable of creating a
variety of tools out of natural objects in order to more easily access water, live food, or to clean themselves. The dental
formula of P. troglodytes and all apes is 2.1.2.3 / 2.1.2.3 = 32 , and the males possess longer canines than the females [6].
Both sexes have a tendency toward baldness, females in particular, and all have heavy brow ridges and prominent ears. The
genitalia of male P. troglodytes is in direct view [5,6].

Figure 5. Pan troglodytes (common chimpanzee) [11]. - To view this image in full size go to the IVIS
website at www.ivis.org . -

The menstrual cycle of P. troglodytes is about 37 days, with estrus lasting ten to 14 days [20]. Mid-cycle ovulation is
marked by pink perineal swelling, signaling increased fertility and the time to mate. Gestation is 228 days, and singletons
are the norm. Weaning occurs after five years, and wild females reach puberty around eight or nine years [5]. In captivity,
great ape females reach menarche around six or seven due to better nutrition [20]. Females produce their first offspring
around 11 or 12 years of age, but males are not fully mature until they reach 15 years of age. The life span for P.
troglodytes in the wild is 50 years [5].

Table 1a. Normative Values for Selected Species of Nonhuman Primates


Macaca mulatta Macaca Papio anubis Pan troglodytes
fascicularis
Mean female wt [8] 3.0 kg 4.0 kg [18] 14 kg [18 ] 31.1 kg
Mean male wt [8] 6.2 kg 6.0 kg [18] 25 kg [18 ] 41.6 kg
Female sexual maturity [1] 2.6 - 3.5 yr 3.0 - 3.4 yr 3 - 4 yr 6 - 7 yr (captive) [20], 8 -
9 yr (wild) [5]
Male sexual maturity[1] 3 - 4 yr 3 - 4 yr 3.5 - 4.5 yr 15 yr [5]
Estrous/menstrual cycle 26 - 30 days 28 - 32 days 30 - 37 days 37 days [20 ]
duration [1]
Gestation [1] 165 - 178 days 155 - 165 days 173 - 193 days 228 days [8]
Birth weight [1] 475 g 345 g 865 g 1.756 kg [8]
Age at weaning [1] 7 - 14 mos 12 - 18 mos 6 - 15 mos 5 yr [5]
Interbirth interval [1] 1 yr 1.1 yr 1.5 - 2 yr
Life span [21] 29 yrs 37.1 yrs 30 - 45 yrs 53 yrs
Mean body temp (rectal) [1] 37 - 39 °C 37 - 39 °C 37 - 39 °C 36.7 - 37.8 °C [22 ]
Heart rate [1] (age and sex 98 - 122 bpm, 115 - 243 bpm 85 - 90 bpm, 80 - 150 bpm [22 ]
dependent) 120 - 180 [23] 150 [23 ]
Respiratory rate [1] 35 - 50/min 30 - 54/min 22 - 35/min 35 - 60/min [22]
Daily water intake [1] 400 - 600 ml 350 - 950 ml 1000 - 600 ml
Daily food intake [1] 400 - 600 g 350 - 550 g 1000 - 1500 g
Blood volume[1] 50 - 96 ml/kg 55 - 75 ml/kg 50 - 70 ml/kg
Daily urine excretion [1] 150 - 550 ml 150 - 400 ml
Dentition [24] 2.1.2.3 / 2.1.2.3 2.1.2.3 / 2.1.2.3 2.1.2.3 / 2.1.2.3 2.1.2.3 / 2.1.2.3
Chromosomes [24] 2n=42 2n=42 2n=42 2n=48
Common Blood Groups [8] O, A, B, AB O, A, B, AB O, A, B, AB O, A
P.anubis, P.
papio
Table 1b. Normative Values for Selected Species of Nonhuman Primates
Callithrix jacchus Saguinus oedipus Aotus trivargatus Saimiri sciureus
Mean female wt [8] 290 g 510 g 1.0 kg 580 g
Mean male wt [8] 310 g 450 g 920 g 750 g
Female sexual maturity [1] 1.5 - 2 yr 1.5 - 2 yr 2.5 - 3.5 yr
Male sexual maturity [1] 1.5 - 2 yr 1.5 - 2 yr 3.5 - 5 yr
Estrous/menstrual cycle duration 28 days 15 days 8 - 10 days
[1]
Gestation [1] 144 days 166 days 133 days [8] 148 - 160 days
Birth weight [1] 27 g 44 g 98 g [8] 95 - 110 g
Age at weaning [1] 2 - 6 mos 2 - 6 mos 6 mos
Interbirth interval [1] 0.5 yr 0.6 yr 1 yr
Life span [21] 12 yrs 13.5 yrs 20 yrs 21 yrs
Mean body temp (rectal) [1] 36.1 - 39.2 °C 38.7 - 39.8 °C
[22 ]
Heart rate [1] 194 - 242 bpm 215 - 263 bpm
Respiratory rate [1] 20 - 50/min [22] 55 - 58/min
Blood group (%) [8]
O 0.0 18.0
A 100.0 55.0
B 0.0 0.0
AB 0.0 27.0

Reproduction
Primate Genitalia and Sexual Differentiation
Male primates, with some exceptions (humans, tarsiers, and spider and woolly monkeys), possess a small bone within the
penis, the os penis. The penis is pendulous and the testes scrotal; the scrotum lies on the sides of the penis in callitrichids
and a few others. In some female New World species (Spider Monkey) the clitoris is pendulous, resembling the penis,
which can make sexual differentiation difficult. Young New World monkeys of both genders possess external genitals of
similar size, in part because female squirrel monkeys and callitrichids possess a pudendal pad. For sexual differentiation,
look for a vulva in females; they also will have a shorter anogenital space than their male counterparts. The genitals can be
manipulated to reveal a slit-like female vaginal opening or a round preputial opening (male). In Saimiri, the clitoris is
covered with horny denticles, giving it a hardened, rough texture [1,5,6,8].

Copulation
Most quadrupedal primates copulate with the male mounting the female from behind. Some brachiators suspend
themselves by their arms or copulate face to face. Pan troglodytes often adopt the quadrupedal position. The females often
initiate mating by presenting their engorged sex skin, which may occur with many partners during estrus. Typically the
dominant (alpha) male fights off the subordinate males only when the females are most fertile, at which time he will
copulate with her. Less dominant males can mate with a female when her fertility is suboptimal [5].

Ovulation
Female primates are born with ovaries containing immature ova that mature as the females undergo puberty. Like humans,
primates spontaneously ovulate according to a regular cycle, and mating is not necessary for ovulation. Estrus occurs when
a female is most fertile around the time of ovulation, and females become more aggressive toward males and are more
likely to engage in sexual activity. The nonhuman primate menstrual cycle is defined as the hormonal and reproductive
tissue changes that occur throughout the reproductive years of the female [20]. In Old World monkeys, estrus is marked by
swelling of the sex skin, and the menstrual cycle ends with sloughing of the uterine lining with blood, at which time the sex
skin will have a less irritated appearance. Swelling of the sex skin involves engorgement of the vulva, thighs, and perineal
region, and sometimes includes hairless areas of the chest, neck, and face. This skin becomes a shiny red and is particularly
friable and easily damaged. New World monkeys do not have genital swelling, and most species do not menstruate [5,8].

Placentation
All Anthropoids have hemochorial placentas in which there is direct contact with maternal blood as the vessels of the
placenta’s outer layer (chorion) burrow into the mother’s uterine vessels. This direct interaction of the mother and fetus’s
circulatory systems optimizes nutrition and oxygenation, while improving waste removal for the fetus, allowing for more
advanced development. During birth, much of the uterine lining and some maternal blood is shed due to the circulatory
connections between mother and fetus; this is referred to as deciduate [5]. All higher primates possess discoid placentas, in
which the chorion attaches over a discoid or round area of the placenta, as opposed to being spread over the placenta ’s
surface, as in nearly all prosimians [8].

Diagnosis of Pregnancy
An experienced diagnostician can often determine gestational age and predict parturition by palpation or ultrasonography.
In callitrichids, the uterus is a four to five millimeter structure at approximately four or five weeks of gestation. In Old
World species, the bi -manual palpation method (See Methodologies section) can be effective as early as 16 days into
pregnancy [1].
Ultrasonography can be utilized at a similar time, but it can be further used in research and in identification of congenital
diseases. Ultrasound is believed to be quite accurate in the estimation of gestational age using a variety of parameters under
the use of experienced ultrasonographers; refer to Conrad for correlation in Macaca nemestrina [25 ].

Parturition
Birth typically occurs at night, except in the case of the great apes. Labor lasts approximately two hours, and its occurrence
at night protects the mother from being left behind by the group as it travels. Except for marmosets and tamarins, single
infants are typical, and the chance of survival is greatest for those who are capable of clinging to their parents as they swing
through the canopy. In the case of the great apes, however, the offspring need not be so advanced, as the parents spend
some time in a bipedal position and have free hands to carry the offspring [5].

Anatomy
Old World monkeys have similar anatomical structure to humans. New and Old World monkeys have developed unique
anatomical features and functional morphology that allow them to adapt to their host environments [26 ]. A comprehensive
primate anatomy textbook entitled "The Anatomy of the Rhesus Monkey (Macaca mulatta)" [27] has been extensively
referenced in this chapter. Modified examples of the original anatomical illustrations from this text are included in this
chapter (Fig. 6 - Fig. 29).

Figure 6. Illustration of the pectoral and abdominal musculature of the rhesus monkey [27] - To view
this image in full size go to the IVIS website at www.ivis.org . -

Figure 7. Illustration of the left pelvic floor of an adult rhesus monkey brain [27]. - To view this image
in full size go to the IVIS website at www.ivis.org . -

Figure 8. Illustration of the superficial back muscles of the rhesus monkey [27]. - To view this image
in full size go to the IVIS website at www.ivis.org . -
Figure 9. Muscles of the right scapula upper arm and forearm, medial view [27]. - To view this image
in full size go to the IVIS website at www.ivis.org . -

Figure 10. Illustration of muscles of the right scapula upper arm and forearm, lateral view [27 ]. - To
view this image in full size go to the IVIS website at www.ivis.org . -

Figure 11. Muscles of the right leg and dorsum of the foot, lateral view [ 27]. - To view this image in
full size go to the IVIS website at www.ivis.org . -

Figure 12. Muscles of the right leg and foot, medial view [27 ]. - To view this image in full size go to
the IVIS website at www.ivis.org . -

Figure 13. Illustration sagittal section of the head and neck [27]. - To view this image in full size go to
the IVIS website at www.ivis.org . -

Figure 14. Illustration of the contents of the thorax of the rhesus monkey [ 27]. - To view this image in
full size go to the IVIS website at www.ivis.org . -
Figure 15. Illustration of the right of the rhesus monkey [ 27]. - To view this image in full size go to the
IVIS website at www.ivis.org . -

Figure 16. Anterior view of the stomach of the rhesus monkey [27]. - To view this image in full size
go to the IVIS website at www.ivis.org . -

Figure 17. Illustration of the intestines of the rhesus monkey [27]. - To view this image in full size go
to the IVIS website at www.ivis.org . -

Figure 18. Illustration of the liver of the rhesus monkey [27]. - To view this image in full size go to the
IVIS website at www.ivis.org . -

Figure 19. Dissection of the penis and the accessory genital glands of the adult male rhesus monkey
[27 ]. - To view this image in full size go to the IVIS website at www.ivis.org . -

Figure 20. Midsaggital view of the pelvic organs of and adult rhesus female monkey [27]. - To view
this image in full size go to the IVIS website at www.ivis.org . -

Figure 21. Illustration of the heart of the rhesus monkey [27 ]. - To view this image in full size go to
the IVIS website at www.ivis.org . -
Figure 22. Illustration of the right subclavian artery and its branches [27]. - To view this image in full
size go to the IVIS website at www.ivis.org . -

Figure 23. External carotid artery and its branches [27]. - To view this image in full size go to the IVIS
website at www.ivis.org . -

Figure 24. Vasculature of the rhesus monkey kidney [27]. - To view this image in full size go to the
IVIS website at www.ivis.org . -

Figure 25. Illustration of the right femoral artery and its branches [27 ]. - To view this image in full size
go to the IVIS website at www.ivis.org . -

Figure 26. Illustration of the thyroid gland and its vasculature [ 27]. - To view this image in full size go
to the IVIS website at www.ivis.org . -

Figure 27. Blood supply of the rhesus monkey adrenal gland [ 27]. - To view this image in full size go
to the IVIS website at www.ivis.org . -

Figure 28. Illustration of the rhesus monkey brain . - To view this image in full size go to the IVIS
website at www.ivis.org . -
Figure 29. Deep nerves of the right eye of the rhesus monkey [27 ]. - To view this image in full size go
to the IVIS website at www.ivis.org . -

Primate Behavior
Normal Behavior
In wild primates, the normal behavioral repertoire is extremely large and varied. Most of these behaviors are not exhibited
in captivity because of restrictions placed on the animal's activity, social interactions, sexual contact, etc. As a rule,
primates housed in groups and provided with an enriched environment exhibit more species-typical behaviors than do
individually housed animals (See Primate Caging and Housing).
Another general rule applicable to the use of laboratory reared animals: in laboratory-bred animals, normal behavior is
fostered by normal maternal contact and normal peer contact. Early weaning, hand rearing and nursery rearing often result
in the appearance of abnormal behaviors. With respect to the behavior of primates in the laboratory setting, rearing
conditions become important factors in animal selection because of increasing reliance on domestically raised primates
[28 ]. Recognition of self by primates was thought to be limited to great apes. Recent studies show this not to be true
[29,30]. General categories and examples of different types of nonhuman primate behavior are referenced in Table 2 in this
online book chapter.

Table 2. Normal Behaviors


Social Agonistic Individual Sexual [31] Maternal
Contact: touching and misc. Bite: involving loss of Forage Mount [32 ] Ventral-ventral
social behavior skin or distal portion of contact posture
the fingers, toes or tails
Groom [33] Slap Eat Mount-thrust Support posture
Embrace Hit Drink Intromission [32] Clutching-
similar to
support but
more firm
Play Grab Rest Genital Retrieval
Manipulation posture
Huddle Poke Travel Dip-sniff Nipple contact
Proximity: maintaining Yawn Passive Female teeth
closeness with no physical chattering
contact
Lip smacking: indicates Stare threat: related to Automanipulate Ejaculation [32 ]
friendliness, affection or hostility, aggression,
interest; one of the first facial attack or dominance, as is
expressions to develop open mouth threat
Fear grimace: related to Charge Vocalize Visual Inspection
withdrawal, flight or
submission
Wide -eyed stare : indicates Push Self-play Hip raise (forced
affection, interest or lifting of
curiosity; seen in most hindquarters
neonates
Table 2. Normal Behaviors
Social Agonistic Individual Sexual [31] Maternal
Quick glance: related to fear Open mouth threat: accompanied Hip touch
grimace, seen with screech by furrowed brows and head
vocalization bobbing
Vocalization: consist of harsh Harsh noises: includes barks, Male teeth
noises and clear calls. growls, moans and explosive chattering
coughs
Oral contact
Sniff
Pursue
Hindquarter
Presentation
Avoid
Flee
Male groom
Female groom

Abnormal Behavior
The term "abnormal behavior" refers to behavioral pathologies. Two classes of behavioral pathologies are recognized:
qualitative abnormalities and quantitative abnormalities [34]. Qualitative abnormalities are behavioral pathologies that
occur in captivity but not in natural settings. Quantitative abnormalities are behavioral pathologies that occur more or less
often in captivity than in natural settings [31 ,34-50].

Table 3. Qualitatively and Quantitatively Abnormal Primate Behaviors


Abnormal Behaviors
Qualitative Quantitative
Bizarre Stereotyped Appetitive Sexual Appetite Activity Agonistic
postures motor acts Disorders Disorders Disorders Behaviors
Floating Stereotyped Coprophagy Inappropriate Hypophagia Hyperactivity- Agonistic
limb Pacing orientation stereotyped Disorders
behavior
Self-biting Head tossing Paint eating Homosexual Hyperphagia Inactivity-
and pica Behavior depression and
apathy
Self- Weaving Sexual Polydipsia
clasping dysfunction
Saluting Bouncing Autoerotic
(eye stimulation
poking)

Nutritive Requirements
Commercial diets are available and preferred in the laboratory setting. Also available are high -fiber diets, dental calculus-
reducing chows, and milk replacers for infants. The standard laboratory nonhuman primate diets provide a balanced supply
of nutrients and vitamins, with supplementation of vitamins D 3 and C (ascorbic acid). Old World monkeys are able to
metabolize vitamin D 2 into vitamin D 3 , unlike New World species, which require dietary vitamin D 3 . Nonhuman primates
require vitamin C, which is oxidized in aqueous solutions and is degradable under a number of conditions (exposure to
light, heat, and some metals). Thus, animals that are fed chow that is exposed to any of these conditions may require
additional vitamin C supplementation. Chow that contains vitamins A, C, or E should not be exposed to high temperatures,
trace minerals, or moisture and should be consumed within 90 days of production [1,51]. New World monkeys typically
receive a diet containing about 25% protein, while Old World species need about 15% protein [1]. Exact information
regarding recommended nutrient needs for a particular captive species is available in Nutrient Requirements of Nonhuman
Primates, 2003 [4].

Supplemental Food Items


The provision of insects in the laboratory setting can be a good source of protein and calcium (insects should be fed a
special calcium-rich diet beforehand, which will be deposited in the gut), particularly for species whose diets typically
include invertebrates. Mealworms and crickets can be used for supplementation and as part of enrichment programs
(foraging). Daily supplementation with fruit and vegetables is also encouraged to provide nutrients and enrichment,
although too much of these can crowd essential nourishment out of the diet of some smaller animals. Care must be taken,
though, to ensure that fruit and vegetables are washed well and are from a quality source, where they have been packed in
order to prevent contamination. All food and supplemental items must be stored in air-tight containers that are on a regular
sterilization schedule [1,4].

Water Requirements of Nonhuman Primates


As a general rule, it is recommended that nonhuman primates have ad libitum access to safe drinking water. Younger
primates, particularly infants, require more water on a daily basis than adult and elderly primates. Smaller species have also
been shown to have greater water requirements than others. Additionally, water needs depend upon room temperature,
humidity, food composition, and the particular animal’s health and activity level. In the event of an experimental
requirement to limit water intake, care should be taken to establish an appropriate water volume to maintain the health of
the animals, and to ensure the integrity of the study. For M. mulatta maintained on a commercial feed, the daily water
requirement is approximately 80 ml/kg body weight [4,52,53].

Diets of New World Monkeys


Supplemental feeding in the laboratory setting with fruits and vegetables, and sometimes insects, is encouraged to provide
variety and additional fiber, fat, and carbohydrates. In the wild, some Callithrix spend much of their days foraging for
insects, which therefore dominate their diets, followed by a large amount of fruit and some exudates (gums). Others,
including C. jacchus, primarily eat exudates and insects, which is supplemented with fruit and nectar [4]. Marmosets have
incisors that are the same length as their canines, which allow them to gouge tree bark with their lower teeth to get to the
exudates. Tamarins possess longer incisors, as exudates play a much smaller dietary role [8]. Saguinus and Leontopithecus
have similar diets dominated by insects and fruit, along with exudates and nectar on a seasonal basis; Saguinus also have a
low intake of young leaves and seeds [4]. Saimiri primarily eat insects, and they are efficient foragers. Fruit plays a smaller,
but significant, role in the diet of the squirrel monkey, along with small amounts of flowers, leaves, seeds, nuts, and figs
(dry season). Aotus are mostly frugivorous, enjoying a fiber-rich diet of leaves and ripe fruit, along with some insects and
flowers. Of greatest importance when feeding nonhuman primates in the laboratory setting is providing a balanced diet that
meets their nutritive needs. It should be noted that fruits in the wild tend to contain more protein than fruit that has been
cultivated for human use, which should be accounted for when establishing proper diets for nonhuman primates [4].

Digestive Tracts of New World Monkeys


An additional trait to consider when establishing diets for nonhuman primates is their digestive anatomy. Many New World
monkeys, including those that figure prominently in research, are combinations of faunivores and frugivores. Marmosets
possess relatively uncomplicated digestive tracts, including stomachs with globular fundi and cylindrical pylori. Aotus and
Saimiri have expanded and haustrated colons, but the cecum is uninvolved [4]. Some species have more difficulty than
others in digesting certain food, yet monkeys used regularly in research tend to be more adaptable to the different diets.

Diets of Old World Monkeys


Macaca fascicularis are true omnivores that subsist mostly on fruit in the wild, along with leaves, prey items, flowers, bark,
roots and other plant matter. Macaca mulatta prefer leaves and fruit, along with a variety of plant matter and prey. Papio
sp. tends to subsist on fruit and seeds, plus various plant derivatives; they have also been known to raid farms and beg from
tourists. Fruit dominates the diet of P. troglodytes in the wild, supplemented with leaves and other plant items, and prey
includes other monkeys [4].

Digestive Tracts of Old World Monkeys


Cercopithecine primates, including Papio and Macaca species, have smooth-walled stomachs with short small intestine.
Their haustrated ceca possess three teniae, allowing for fermentation of plant cellulose by certain symbiotic bacteria in
areas distal to digestive enzymes. Macaca also have enlarged ceca and colons to slow passage of fiber-rich plant matter to
aid in fermentation. The presence of cheek pouches in these primates allows additional time for digestive enzymes in saliva
to begin the digestive process. The Pan colon is haustrated, as is the relatively small cecum, with three teniae, which
terminate in an appendix at the proximal end of the cecum, which also allows for some fermentation to occur in the hindgut
[4].

Normative Hematology
Tables four through seven in this chapter provide the more common reference ranges for reported for both New and Old
World Primates. The reader should note that normal hematological parameters for nonhuman primates can be influenced by
a wide rage of factors (age, gender, housing status, etc). See Table 4 (located at the end of the document) and Table 5.

Table 5. New World and Old World Monkey Blood Chemistry Values
Analyte Units Callithrix Owl Rhesus Cynomologus Baboons Chimpanzee
jaccus adults Monkeys macaque monkeys
(fasted)
Glucose mg/dL 126 139+/- 35 53 - 87 42 - 111 80 - 95 62 - 94
Uric Acid mg/dL 4,1 - 0.2 +/- 0.1 0.1 - 0.3 - -
BUN mg/dL 27 15 +/- 5.4 14.2 - 19.6 5.0 - 25.0 8.0 - 14.0 9.0 - 19.0
Urea mg/dL - - - - - -
Creatinine mg/dL - 1.0 +/- 0.4 0.9+/- 0.2 0.5 - 1.3 1.0 +/- 0.8 - 1.3
0.5
TBili mg/dL 0,5 0.8 +/- 0.4 0.10 - 0.66 0.1 - 0.5 0.3 - 0.4 0.06 - 0.28
Dir. Bili mg/dL 0,2 - - - - -
Ind. Bili mg/dL 0,3 - - - - -
TP mg/dL 7 8.3 +/- 0.9 7.3+/- 0.4 6.5 - 8.7 6.0 - 7.0 6.7 - 8.1
Albumin mg/dL 3,8 4.4 +/- 0.5 4.6 +/- 0.3 2.6 - 3.4 3.5+/- 1.4 3.3 - 4.1
Globulin mg/dL 3,2 - - 2.1 - 5.9 3.6 +/- 3.2 - 4.7
1.1
Cholesterol mg/dL - 150 +/- 46 94 - 162 42 - 210 60 - 134 161 - 257
ALP IU/L 2,4 494 +/ - 541 +/- 144 62 - 680 248 +/- 54 - 153
469 303
AST IU/L 160 - 20 - 34 16 - 64 22 - 28 4.0 - 13.0
(SGOT)
ALT IU/L 60 47 +/- 37 145 - 171 11.0 - 88.0 12.0 - 1.4 - 10.0
(SGPT) 20.0
LDH IU/L 799 - 201 - 665 174 - 975 244 - 203 - 503
1100
GGT IU/L - 17 +/-14 57 +/- 20 - 39+/- 22 oct-35
Calcium mg/dL 9,5 10.4 +/- 10.7+/ - 0.6 8.3 - 10.9 8.0 - 10.0 8.0 - 10.0
1.0
Phosphate mg/dL 6,9 4.0 +/- 1.5 4.0 - 6.0 1.4 - 6.7 5.5 - 8.5 3.6 - 6.0
Na mEq/L - 152 +/ - 5 6.1 - 7.1 135 - 154 149 +/- 5 136 - 148
Table 5. New World and Old World Monkey Blood Chemistry Values
Analyte Units Callithrix jaccus Owl Rhesus Cynomologus Baboons Chimpanzee
adults (fasted) Monkeys macaque monkeys
K mEq/L - 3.8 +/- 0.7 5.7 - 1.0 3.4 - 6.3 3.9 +/- 3.2 - 4.4
1.1
Cl mEq/L - - 113 +/ - 2 97 - 113 99 +/- 8 93 - 115
Note: Macaca mulatta (Rhesus macaque) and Macaca fascicularis (Cynomologus macaque) parameters taken from
3 - 4 year old male parameters [1,55,56].

Husbandry and Management


Given their advanced physical and mental functioning, nonhuman primates require a great deal of care. They are capable of
advanced manipulation with their extremities, to the extent of being able to escape from their housing, and their mental
capability places them in the unique position of being able to troubleshoot problems, but may also predispose them to
behavioral issues and stereotypes. In order to maintain the mental and physical health of nonhuman primates, their daily
routine must include an extensive list of interactions as is discussed in the following sections and the "Guide for the Care
and Use of Laboratory Animals" (the "Guide"), or as established by the USDA under the Animal Welfare Act (P.L. 89-544,
92-579, 94-279) [53,54,57].
Basic standards are identified that govern the minimum quality of material that will be involved with the animals and their
care, including water, food, storage, waste disposal, sinks, ventilation, etc. and are defined in the "Guide" [53 ].

Nonhuman Primate Quarantine Procedures


The quarantine time for nonhuman primates after their arrival varies upon the institution. However, some institutions may
shorten or lengthen their quarantine depending on the animals’ source and their internal quarantine procedures. A typical
nonhuman primate quarantine period range from 31 to 90 days. The purpose of quarantine is to protect against the
introduction of foreign disease that is not endemic to a population, and it allows for the evaluation of the primates’ health
for the protection of their human handlers. It also gives the new animals an opportunity to settle into their new environment
before being introduced to a larger group of nonhuman primates where there will be more social stressors. The veterinary
staff uses the quarantine period for a number of procedures. Tuberculin skin test (TST) should be given every two weeks in
alternating eyelids (intrapalpebral administration), beginning the day after the animal arrives. A majority of primate
vivarians require at least 3 consecutive negative-skin tests performed every 2 weeks before releasing primates from
quarantine. Follow-up tests should be given at the end of months two and three. The skin on the abdomen is also used
sometimes as a visible location for TB tests (for TB test administration and interpretation See Methodologies section),
particularly when there is bruising on the eyelid that can obscure or interfere with reading the result of the test. A recently
recommended protocol for TB testing suggest parallel use of a whole blood Mycobacterium tuberculosis gamma interferon
assay (Primagam tm ) with the intradermal test in order to diagnose Tuberculosis in primates. Interferon –gamma (IFN ?)
cytokine levels increase in the presence of tuberculin antigens [58,59]. Both test have been shown to have variable
sensitivity (Primagam tm 68% versus TST 84%) and specificity (Primagam tm 97% versus TST 87%), thus validating the
recommendation for parallel testing [60 ].

Also on the day after arrival, the veterinary staff should anesthetize the animals and examine, weigh and tattoo them for
identification. Additionally, the staff should obtain a fecal sample from New World species in order to identify any specific
anti-parasitic agents that may need to be given. Old World species are generally given a prophylactic subcutaneous dose of
ivermectin (200 µg/kg body weight) as an antihelminthic [ 61]. A thoracic radiograph can be performed at this time if a
recent radiograph of good quality was not sent by the animal ’s supplier to verify that the lungs are clear of lesions. Baseline
blood work should also be done soon after the animals arrive at the facility to establish a file, and body weight should be
monitored every time an animal is anesthetized. A necropsy should be performed on any animal that dies during the
quarantine period.

Feeding During Quarantine


Each animal’s food intake should be monitored during its first month of quarantine, and its food should be rationed over the
first week. Clinical veterinarians should be consulted regarding specific quarantine procedures for any species of
nonhuman primate. Rhesus monkeys eat approximately four percent of their body weight per day and should be fed the
appropriate number of biscuits based on guidelines outlined in Table 6, and this daily ration should be divided into two or
more daily feedings. All newly quarantined nonhuman primates should be evaluated routinely (excessive food wastage,
obesity, weight loss, general body condition).
Table 6. Nonhuman Primate Feeding Chart [62]
# Biscuits per day # Biscuits per day
Weight in Weight in
(4/Kg of Body Wt) (4/Kg of Body
Kg Kg
@ Wt)
2.0 8 11.5 46
2.5 10 12.0 46
3.0 12 12.5 50
3.5 14 13.0 52
4.0 16 13.5 54
4.5 18 14.0 56
5.0 20 14.5 58
5.5 22 15.0 60
6.0 24 15.5 62
6.5 26 16.0 64
7.0 28 16.5 66
7.5 30 17.0 68
8.0 32 17.5 70
8.5 34 18.0 72
9.0 36 18.5 74
9.5 38 19.0 76
10.0 40 19.5 78
10.5 42 20.0 80
11.0 22 *
*Adolescent rhesus monkeys require approximately 100 Kcal/kg.
Adult rhesus monkeys (>7 years) require 50 - 70 Kcal/kg (heavier
animals require less caloric intake per kg). @ Purina Monkey Chow
#5038 and High Protein Monkey Chow #5045 (Lab Diet®, PMI®
Nutrition International, LLC, Brentwood, MO) have 3.4
"physiological" Kcal/gm, and each biscuit weighs approximately 7.6
gm; thus each biscuit contains approximately 26.6 "physiological"
Kcal. This calculates to 3.76 (4) biscuits fed per kg body weight for an
adolescent rhesus monkey, down to 2.26 (2) biscuits per kg for an adult
minimum.

Nonhuman Primate Caging and Housing


Overall, primate housing systems must facilitate animal well -being, meet research requirements, and minimize
experimental variables. In the primary enclosure the temperature, humidity, and composition of air within it constitute the
microenvironment. The secondary enclosure, such as a room or barn constitutes the animal’s macroenvironment [63 ].
Detailed regulations regarding nonhuman primate housing environments and space recommendations are outlined in the
NRC "Guide" of 1996, and AWA Standards [53 ,57].

The space requirements outlined in the "Guide for the Care and Use of Laboratory Animals" and Table 7 is the minimum
space that facilities must provide for their nonhuman primates. Table 8 includes the recommendations outlined by the
Animal Welfare Act (AWA), which provides larger suggested enclosure dimensions for all animals over 25 kilograms;
some institutions require their investigators to meet the stricter standards of the AWA. The groupings provided are based
upon the typical weight for various species. In general, weight changes due to pregnancy or obesity should not require a
change in cage size, unless the animal is unable to make normal postural adjustments and movements within the enclosure.
Infants and juveniles of certain species are often lower in weight than adults of those species and can be housed under the
space guidelines for smaller species, unless the animal is obviously unable to make normal movements within the enclosure
[53 ,57].

Table 7. Minimum Housing Requirements for Nonhuman Primates ("Guide") [53]


Group Weight Floor area/ Height
animal
Monkeys [a] lbs kg ft 2 m2 in cm
Group 1 Up to 2.2 Up to 1 1.6 0.15 20 50.8
Group 2 Up to 6.6 Up to 3 3 0.28 30 76.2
Group 3 Up to 22 Up to 10 4.3 0.41 30 76.2
Group 4 Up to 33 Up to 15 6 0.57 32 81.3
Group 5 Up to 55 Up to 25 8 0.75 36 91.5
Group 6 Up to 66 Up to 30 10 0.94 46 117
Group 7 >66 >30 15 1.41 46 117
Apes (pongidae) [b] lbs kg ft 2 m2 in cm
Group 1 Up to 44 Up to 20 10 0.94 55 140
Group 2 Up to 77 Up to 35 15 1.41 60 152
Group 3 >77 >35 25 2.33 84 213
a Callitrichidae, Cebidae, and Cercopithecidae, including Papio. Baboons might require

more height than other monkeys.


b For some genera (e.g., Brachyteles, Hylobates, Symphalangus, Pongo , and Pan), cage

height should be such that an animal can, when fully extended, swing from the cage
ceiling without having its feet touch the floor. Cage-ceiling design should enhance
brachiating movement.

Table 8. Primary Enclosure Recommendations for Nonhuman Primates (Animal Welfare Act Regulations)
[57,64]
Group c Weight Floor area / animal Height
lbs kg ft 2 m2 in cm
1 Under 2.2 under 1 1.6 0.15 20 50.8
2 2.2 - 6.6 1-3 3 0.28 30 76.2
3 6.6 - 22.0 3 - 10 4.3 0.41 30 76.2
4 22.0 - 33.0 10 - 15 6 0.57 32 81.3
Table 8. Primary Enclosure Recommendations for Nonhuman Primates (Animal Welfare Act Regulations)
[57,64]
Group c Weight Floor area / animal Height
5 33.0 - 55.0 15 - 25 8 0.75 36 91.5
6 Over 55.0 over 25 25.1 2.37 84 214
cSpecies typically included in each group are:
Group 1 - marmosets, tamarins, and infants (less than 6 months of age) of various species.
Group 2 - capuchins, squirrel monkeys and similar size species, and juveniles (6 months to 3 years of age) of various
species.
Group 3 - macaques and African species.
Group 4 - male macaques and large African species.
Group 5 - baboons and nonbrachiating species larger than 33.0 lbs. (15 kg).
Group 6 - great apes over 55.0 lbs. (25 kg), and brachiating species.

There are several other points that should receive consideration when housing options are being evaluated. Long-tailed
species should be provided with enough vertical space to allow the animal to attain a normal upright stance without the tail
leaving the enclosure or falling into waste pans. Additionally, nocturnal species and those that sleep in cavities should be
given nest boxes or nesting material. Finally, due to their size and the difficulty in transferring them between cages, apes
weighing over 50 kg are most effectively housed in permanent housing of masonry, concrete, and wire -panel structures,
rather than in conventional caging [53,57].

Additional Housing Options


Outdoor group housing: Outdoor housing is most useful in semitropical and tropical areas. Commonly used outdoor
enclosures are corn cribs, runs, islands, corrals, and field cages [65].
Indoor Group and Individual Housing Systems: Individual cages of appropriate size with partitions between cages; cages
can be wall or rack mounted. Racks are usually mounted on casters to allow mobility and sanitation in a cage washer [66-
71]. Space for group-housed animals should be based on individual species needs [72-75 ].

Environmental Enrichment
In the wild, nonhuman primates spend a large amount of their waking time foraging for food, while captive monkeys are
often fed only a couple of times per day. These large amounts of free time that are available to captive nonhuman primates
can allow them the opportunity to develop behavioral conditions that include hair pulling, cheek chewing, and other
repetitive and self-destructive acts.
Therefore, the development of enrichment programs for nonhuman primates has become federally regulated. Institutions
need to implement plans, based on the species of nonhuman primates that they house, that work with the experimental
ideals while providing the animals with daily means of interacting with their environments. There are two forms of activity,
each with unlimited possibilities. The first is foraging, which involves seeking food (Fig. 30) [76 ].

Figure 30. Rhesus monkeys foraging for food in enclosure [11 ]. - To view this image in full size go to
the IVIS website at www.ivis.org . -

This can be in the form of foraging boards containing raisins, seeds, or insects; tubes containing exudates; or puzzle feeders
containing a variety of fruit pieces. A primate ’s chow can be scattered on the top of its cage with or without straw or
another material to prolong the animal’s time spent feeding. Seeds can be placed in clean plastic bottles containing peanut
butter or molasses; primates enjoy uncapping these and creating tools to withdraw their treat. The other option is in the
form of enrichment, which is typically inside the animal’s cage or attached by a chain or cable, which allows the animal to
play when it desires (Fig. 31) [76].

Some forms of enrichment are toys in the cage -many are large chew toys or balls produced for dogs, but can be as simple
as a section of log to chew or a section of PVC pipe with capped ends. Consideration should be given to the time and cost
of materials required to prepare foraging boards and puzzle feeders and the ease and ability of sanitizing implements for
other animals’ use.
Foraging equipment should be cleaned between each use and effort should be make to rotate different materials and puzzles
among animals to provide variety, as these species quickly learn to solve puzzles [29 ,37,38,43,44,46,49 ,69-71,77 -150].

Figure 31. Rhesus monkeys on jungle gym [11 ]. - To view this image in full size go to the IVIS
website at www.ivis.org . -

Primate Reuse and Retirement


Given the great expense and controversial nature of nonhuman primate research, it should be mentioned that there are a
number of uses for nonhuman primates when they are no longer needed by a particular laboratory or institution.
Often, when a necropsy is not necessary to evaluate the after effects of a study, a nonhuman primate can be sold to another
accredited institution for additional research use, thus reducing the number of nonhuman primates required for biomedical
use. Regardless of the choice made, the animals should be provided care following the guidelines set forth under the
Animal Welfare Act and under the supervision of the United States Department of Agriculture (See Resources Section).

Management
Legal Considerations of Research Using Nonhuman Primates
Nonhuman primates are protected in the United States under the Animal Welfare Act and its amendments. Any entity that
is purchasing, transporting, or conducting experiments on animals covered under the Act must be registered with the United
States Department of Agriculture (USDA). Research facilities must submit annual reports to the USDA regarding
appropriate use of anesthesia, analgesia, and tranquilizers during experimentation. Facilities must keep official records and
tags for their own identification and have it on hand for USDA inspection for as long as one year after an animal’s death.

Transporting Nonhuman Primates


All nonhuman primates are protected under the Convention on International Trade in Endangered Species of Wild Fauna
and Flora (CITES) treaty, and thus must be cared for under stringent guidelines. Nonhuman primates must be accompanied
by a health certificate when they are being transported, and a strict set of guidelines must be followed in their transport. A
nonhuman primate in transit must not be exposed to temperature extremes above 29.4 ° C (85 °F) or below 7.2 °C (45 °F)
unless an USDA accredited veterinarian has certified that it has been acclimated to temperatures below 7.2 °C within the
past ten days. The thermometer readings must be taken within 91 cm (3 ft) of the animal’s enclosure [151].
Transportation regulations are updated on a yearly basis effective on the first of October of each year, and new editions of
the book Live Animals Regulations are available from the International Air Transport Association (www.iata.org ) [152].

Occupational Health and Safety


Primate zoonoses are a significant public health care concern; therefore it is imperative that humans working with
nonhuman primates understand the risk associated with exposure to them. Two recent publications that provide a
comprehensive review of occupational health and safety issues surrounding nonhuman primates are entitled 1)
"Occupational Health and Safety in the Care and Use of Nonhuman Primates", published by The National Research
Council (NRC) [153], and 2) "Zoonoses of Occupational Health Importance in Contemporary Laboratory Animal
Research", by Hankenson et al. [154].
It is strongly recommended by the authors that any individual or entity working directly with nonhuman primates have a
working knowledge of these publications.

Personal Protective Equipment


All species that are commonly used in the laboratory are capable of sharing diseases (zoonoses) with their human handlers,
so great caution must be taken to protect the well-being of both. All personnel (husbandry, veterinary, and investigative)
must have had a negative TB test less than six months prior to contact with any nonhuman primate, as nonhuman primates
are extremely susceptible to the disease. Each institution should establish standard procedures for personal protective
equipment (PPE) that all personnel must follow. These vary by species, as the degree of severity of zoonoses risk changes.
Animals in quarantine are to be handled as if they are positive for diseases such as tuberculosis and herpes B virus, thus, all
personnel must wear proper attire: long pants, lab coat or gown, mask, gloves, shoe covers, and appropriate eye protection
(seal around the eye- goggles or face shield). An additional pair of gloves is preferable.
Following quarantine, a mask and gloves are typically sufficient, as long as the animals or their excrement are not actually
being handled. In the case of macaques, however, all of the above listed PPE is required at all times, as they are common
carriers of herpes B, virus [61]. To avoid cross-contamination, known herpes B -positive animals should be housed in the
same room, with staff visiting after completing tasks in other rooms if possible.
Equipment sharing between housing rooms should be avoided as well. Additional protective equipment is available for
work with macaques and other high-risk or particularly dangerous animals; including steel mesh gloves, Kevlar wrist and
arm shields, and poles that allow handlers to "jump" animals from one cage to another from a safe distance. Lab coats and
equipment should not be moved from one animal room to another without being disinfected in between, which is
particularly important when animals are in quarantine. Information regarding handling of nonhuman primates is included in
the Methodologies section.

Primate Resources
l Washington National Primate Research Center - http://www.wanprc.org/WaNPRC/
l Yerkes National Primate Research Center - http://www.emory.edu/WHSC/YERKES/
l Southwest National Primate Research Center - http://www.snprc.org/
l California National Primate Research Center - http://www.crprc.ucdavis.edu/
l New England Primate Research Center - http://www.hms.harvard.edu/nerprc
l Oregon National Primate Research Center - http://onprc.ohsu.edu
l Tulane Primate Center - http://www.tpc.tulane.edu
l Wisconsin Regional Primate Research Center - http://www.primate.wisc.edu
l USDA - http://www.usda.gov
l CDC - http://www.cdc.gov
l NIH - http://www.nih.gov
l Association of Primate Veterinarians - http://www.primatevets.org
l Primate Supply Information Clearinghouse - http://wanprc.org/psic/
l Chimp Haven - http://www.chimphaven.org/
l The National Sanctuary for Retired Research Primates (NSRRP) - http://www.primatesanctuarynsrrp.org
l National B Virus Resource Center - http://www.gsu.edu/~wwwvir/index.html
l Atlas of the Primate Brain - http://braininfo.rprc.washington.edu/menumain.html
In: Laboratory Animal Medicine and Management, Reuter J.D. and Suckow M.A. (Eds.).
International Veterinary Information Service, Ithaca NY (www.ivis.org), Last updated: 27-mars-2006;
B2507.0306
Biology and Medicine of Non-human Primates. Part I: Physiology and
Management
M.J. Linn 1 , R. Duran-Struuck 2 , A.K. Trivedi 3 , L.B. Zajic 4 , S.K. Wrobleski 5 , A.E. Hawley 6 and D. D. Myers Jr. 7
2,7 Unit for Laboratory Animal Medicine and 1,3,4,5,6,7 Jobst Vascular Laboratory, Section of Vascular Surgery, Department

of Surgery, University of Michigan Medical Center, Ann Arbor, MI, USA.

Table 4. Normative Hematology for Multiple Primate Species [2,24 ,54]


UNITS Marmoset Squirrel Owl Rhesus Cyanomologous Baboons
and Monkeys Monkeys monkeys monkeys Chimpanzee
Tamarins
C. jacchus S. S. A. M. M. fascicularis Pappio Pan
oedipus scireus trivigartus mulatta sp. Troglodytes
RBC 10 6 /mm 3 6,86 6,59 [5.9 - 5.17+/- 5.02+/- [3.9 - 7.1] 4.5+/-
4.8+/-0.3
9.4] 0.84 0.55 0.5
Hb gm/dL 15,1 15,5 [9.3 - 14.3+/ -1.1 12.9+/- [11.6 - 14.5] 11.4+/ -
12.6+/ -0.9
16.1] 1.81 1.2
PCV % 45 45 [30.5 - 42.0+/ -5.4 39.60+/ - [38 - 50] 36.0+/ -
39.0+/ -2.6
43.6] 3.61 3.6
MCV um 3 67 69 [39 - 82.4+/- 79.48+/ - [69.1 - 90.0] 80.0+/ -
82.0+/ -3.6
60] 11.9 7.48 2.5
MCH ug 22 23 [12.2 - 26.9+/ -3.1 25.93+/ - [21.1 - 26.4] 26.0+/ -
26.0+/ -0.9
21.0] 2.89 0.5
MCHC % 34 34 [24.8 - 34.1+/- 3.1 32.63+/ - [26.4 - 33.0] 32.0+/ -
33.0+/ -1.3
44.2] 2.11 1.3
Table 4. Normative Hematology for Multiple Primate Species [2,24,54 ]
UNITS Marmoset Squirrel Owl Rhesus Cyanomologous Baboons
and Monkeys Monkeys monkeys monkeys Chimpanzee
Tamarins
C. jacchus S. S. A. M. M. fascicularis Pappio Pan
oedipus scireus trivigartus mulatta sp. Troglodytes
WBC’s X10 3 /mm3 10.0+/ -2.7 12,6 [4.6 - 12.7+/ -4.7 8.17+/- [8.15 - 21.3] 7.9 +/-
13.3+/ -4.8
11.7] 3.25 2.6
*
Bands % 1,7 0,4 - - [50+/ - - -
92]-
0.2 *
[276+/ -
476]
Segmented % 37.4+/- 43 [22.5 - 55.4+/ -7.6 37.3+/- [13.8 - 81.0] 44+/-13
61+/ -17
Neut. 14.7 80.0] 9.5
Lymphocytes % 59.9+/- 49 [20 - 35.5+/- 58.8+/- [35 - 83] 46+/-13
35+/ -17
14.7 68] 18.3 15.0
Eosinophils % 0.9+/-0.9 1,2 [0 - 10] 9.5+/-9.2 2.56+/- [0 - 11] 2+/-1
1.0+/-0.9
2.65
Basophils % 0.2+/-0.3 0,1 [0 - 1] <0.1 0.2+/- [0 - 1] 1+/-1
0
0.54
Monocytes % 1.6+/-1.1 5 [1 - 6] - 2.15+/- [1 - 1] 7+/-3.9
2.0+/-1.5
2.21
Platelet 10 3 /mm 3 490 - - 431+/ -119 - [195 - 357] [151 -
[148 - 363]
481]
[ ] = Reference Range
Note: The above mentioned values are the mean or range published in the current literature. For further detail regarding the values
within subspecies and stratification in age groups, please refer to the mentioned references.
*Very variable. Please refer to references for further detail.

All rights reserved. This document is available on-line at www.ivis.org. Document No. B2507.0306
References
1. Fortman JD, Hewett TA, Bennett BT. The Laboratory Nonhuman Primate. Boca Raton, FL: CRC Press, LLC, 2002.
2. Bernacky BJ, Gibson SV, et al. Nonhuman Primates In: Fox JG, Anderson LC, Loew FM, et al., eds. Laboratory Animal
Medicine. 2nd Edition ed. San Diego: Academic Press, 2002; 675-791.
3. Abbott DH, Barnett DK, Colman RJ, et al. Aspects of the common marmoset basic biology and life history important for
biomedical research. Comp Med 2003; 53:339-350.
4. National Research Council. Nutrient Requirements of Nonhuman Primates. 2nd rev. ed. Washington, D.C.: The National
Academies Press, 2003.
5. Napier JR, Napier PH. The Natural History of the Primates. Cambridge, MA: The MIT Press, 1985.
6. Napier JR, Napier PH. A Handbook of Living Primates Morphology, Ecology and Behaviour of Nonhuman Primates.
London: Academic Press, 1967.
7. Layne DG, Power RA. Husbandry, handling, and nutrition of marmosets. Comp Med 2003; 53:351-359.
8. Swindler DR. Introduction to the Primates. Seattle and London: University of Washington Press, 1998.
9. Tardif SD, Smucny DA, Abbott DH, et al. Reproduction in captive common marmosets (Callithrix jacchus). Comp Med
2003; 53:364-368.
10. Strier KB. Primate Behavioral Ecology. Boston, MA: Allyn and Bacon, 2003.
11. Medicine ACoLA. Laboratory Animal Medicine & Science Series II (Version 1.0) [CD-ROM] In: Medicine ACoLA,
ed. Chester, NH: Balk, M. American College of Laboratory Animal Medicine, 2000.
12. Flannery S. Primate Info Net: Northern Owl Monkey: Wisconsin Primate Research Center, 2002.
13. Kumamoto AT, Houck ML. Cytogenetic identification of a hybrid owl monkey, Aotus Nancymaae x Aotus Lemurinus
Griseimembra. J Zoo Wildl Med 2001; 32:130 -133.
14. Flannery S. Primate Info Net: Common Squirrel Monkey: Wisconsin Primate Research Center, 2002.
15. Flannery S. Primate Info Net: Crab-eating Macaque: Wisconsin Primate Research Center, 2002.
16. Flannery S. Primate Info Net: Rhesus Macaque: Wisconsin Primate Research Center, 2002.
17. Bielitzki JT. Integumentary System In: Bennett B, Abee CR, Henrickson RV, eds. Nonhuman Primates in Biomedical
Research: Diseases. San Diego: Academic Press, 1998; 363-375.
18. Flannery S. Primate Info Net: Olive Baboon: Wisconsin Primate Research Center, 2000.
19. Flannery S. Primate Info Net: Hamadryas Baboon: Wisconsin Primate Research Center, 2002.
20. Nadler RD. Monkey Madness: Primate Menstrual Cycle: Yerkes Regional Primate Research Center, Emory University.
21. Rowe N. The Pictorial Guide to Living Primates. East Hampton: Pogonias Press, 1996.
22. Unit for Laboratory Animal Medicine. Guidelines for Anesthesia, Analgesia & Postanesthetic Care of Nonhuman
Primates. Ann Arbor, Michigan: University of Michigan, 2001; 1 -11.
23. OACU. Anesthesia and Analgesia Formulary, version 1/02 In: Use OoACa, ed, 2002.
24. Napier JR, Napier PH. A Handbook of Living Primates: Morphology, Ecology and Behaviour of Nonhuman Primates.
London: Academic Press, 1967.
25. Conrad S, Kroeker R, Ha J, et al. Ultrasound Estimation of Fetal Growth in Macaca Nemestrina.
26. Turnquist J, Hong N. Functional Morphology In: Bennett B, Abee CR,RV. H, eds. Nonhuman Primates in Biomedical
Research: Biology and Management. San Diego: Academic Press, Inc., 1995; 49-76.
27. Bast TH, Kopel B, Christensen K, et al. The Anatomy of the Rhesus Monkey, (Macaca mulatta). New York: Hafner
Publishing Co., 1961.
28. Rush HG. Primate Behavior. Ann Arbor: Unit for Laboratory Animal Medicine, University of Michigan, 2001; 1-15.
29. Gallup GG, Jr., Suarez SD. Social responding to mirrors in rhesus monkeys (Macaca mulatta): effects of temporary
mirror removal. J Comp Psychol 1991; 105:376-379.
30. Hauser MD, Kralik J, Botto-Mahan C, et al. Self-recognition in primates: phylogeny and the salience of species-typical
features. Proc Natl Acad Sci USA 1995; 92:10811-10814.
31. Estep DQ, Bruce KE, Johnston ME, et al. Sexual behavior of group-housed stumptail macaques (Macaca arctoides):
temporal, demographic and sociosexual relationships. Folia Primatol (Basel) 1984; 42:115 -126.
32. Goldfoot DA, Slob AK, Scheffler G, et al. Multiple ejaculations during prolonged sexual tests and lack of resultant
serum testosterone increases in Male Stumptail Macaques (M. arctoides). Arch Sex Behav 1975; 4:547-560.
33. Taira K, Rolls ET. Receiving grooming as a reinforcer for the monkey. Physiol Behav 1996; 59:1189-1192.
34. Erwin J, Deni R. Strangers in a strange land: Abnormal behaviors or abnormal environments? In: Erwin J, Maple TL,
Mitchell GH, eds. Captivity and Behavior: Primates in Breeding Colonies, Laboratories and Zoos. New York: van
Nostrand Reinhold, 1979; 1-28.
35. Weld KP, Mench JA, Woodward RA, et al. Effect of tryptophan treatment on self-biting and central nervous system
serotonin metabolism in rhesus monkeys (Macaca mulatta). Neuropsychopharm 1998; 19:314-321.
36. Bayne K, Dexter S, Suomi S. A preliminary survey of the incidence of abnormal behavior in rhesus monkeys (Macaca
mulatta) relative to housing conditions. Lab Anim 1992; 21:38-46.
37. Bayne KA, Hurst JK, Dexter SL. Evaluation of the preference to and behavioral effects of an enriched environment on
male rhesus monkeys. Lab Anim Sci 1992; 42:38-45.
38. Chamove AR, Anderson JR, et al. Deep woodchip litter: hygiene, feeding, and behavioral enrichment in eight primate
species. Int J Stud Anim Probl 1982; 3:308 -318.
39. Erwin J, Mitchell GH, Maple T. Abnormal behavior in non -isolate -reared rhesus monkeys. Psychol Rep 1973; 33:515-
523.
40. Erwin J, Mitchell GH. Initial heterosexual behavior of adolescent Rhesus monkeys (Macaca mulatta). Arch Sex Behav
1975; 4:97-104.
41. Judge PG, de Waal FB, Paul KS, et al. Removal of a trauma-inflicting alpha matriline from a group of rhesus macaques
to control severe wounding. Lab Anim Sci 1994; 44:344-350.
42. Crockett CM, Bowers CL, Shimoji M, et al. Behavioral responses of longtailed macaques to different cage sizes and
common laboratory experiences. J Comp Psychol 1995; 109:368-383.
43. Lam K, Rupniak NM, Iversen SD. Use of a grooming and foraging substrate to reduce cage stereotypies in macaques. J
Med Primatol 1991; 20:104-109.
44. Line SW, Clarke AS, Markowitz H, et al. Responses of female rhesus macaques to an environmental enrichment
apparatus. Lab Anim 1990; 24:213-220.
45. Mitchell GH, Clarke AS. Contributions of behavioral primatology to veterinary science and comparative medicine. Adv
Vet Sci Comp Med 1984; 28:25-50.
46. Renquist DM, Judge FJ. Use of nylon balls as a behavioral modifier for caged primates. Lab Primate Newsletter 1985;
24:4.
47. Schapiro SJ, Lee-Parritz DE, Taylor LL, et al. Behavioral management of specific pathogen-free rhesus macaques:
group formation, reproduction, and parental competence. Lab Anim Sci 1994; 44:229 -234.
48. Suomi SJ, Harlow HF. Depressive behavior in young monkeys subjected to vertical chamber confinement. J Comp
Physiol Psychol 1972; 80:11-18.
49. Tolan JC, Malone DR, et al. An exercise cage for monkeys. Lab Primate Newsletter 1980; 19:3-5.
50. Champoux M, Suomi S, Schneider ML. Temperament differences between captive Indian and Chinese-Indian hybrid
rhesus macaque neonates. Lab Anim Sci 1994; 44:351-357.
51. McDowell, Russell L. Vitamins in Animal and Human Nutrition. 2nd ed. Ames, IA: Iowa State University Press, 2000.
52. Richter CB, Lehner NDM, Henrickson RV. Primates In: Fox JG, Cohen JB,Loew FM, eds. Laboratory Animal
Medicine. Orlando: Academic Press, 1984; 297-383.
53. Committee on the Care and Use of Laboratory Animals, Institute of Laboratory Animal Resources. Guide for the Care
and Use of Laboratory Animals. Washington, D.C.: National Academy Press, 1996.
54. Howell S, Hoffman K, Bartel L, et al. Normal hematologic and serum clinical chemistry values for captive
chimpanzees (Pan troglodytes). Comp Med 2003; 53:413 -423.
55. Fox JA, L. Loew, F. Quimby, F. Laboratory Animal Medicine. 2nd edition ed: Academic Press, 2002.
56. Carpenter JW, Mashima TY, Rupiper DJ. Exotic Animal Formulary. Second ed: W. B. Saunders Company, 2001.
57. Animal Welfare Act. HR. 89 ed.
58. Collins HL, S. H. Kaufmann. The many faces of host responses to tuberculosis. Immunology 2001:1-9.
59. Dannenberg AM, Jr. Pathogenesis of pulmonary Mycobacterium bovis infection: badis principles established by the
rabbit model. Tuberculosis (Edinb) 2001:87-96.
60. Garcia Y, Bouley, Moorhead, and Lerche. Diagnosis of tuberculosis in Macaques, Using Whole-Blood In Vitro
Interferon-Gamma (PRIMAGAM) Testing. Comparitive Medicine 2004; 54:86-92.
61. Dysko RC. Nonhuman primate quarantine procedure. Ann Arbor, MI: Unit for Laboratory Animal Medicine,
University of Michigan, 1998; 1-4.
62. Day G, Decoster J, Dysko R. Guideline for feeding chow to primates. Ann Arbor, MI: Unit for Laboratory Animal
Medicine, University of Michigan, 1996; 1-2.
63. Kempa WR. Primate Medicine and Biology: Caging and Housing Part -1. Ann Arbor: Unit for Laboratory Animal
Medicine, University of Michigan, 2003; 1-27.
64. Reuter JDMAS. Regulatory Compliance. Ithaca: International Veterinary Information Service, 2003. - Available from
www.ivis.org , Sep. 30, 2000. -
65. Cary ME, et al. Effects of confinement environment on reproductive efficiency in the baboon. Contemp Top Lab Anim
Sci 2003; 42:35-39.
66. Hartner M, Hall J. Group housing subadult male cynomolgus macaques in a pharmaceutical environment. Lab Anim
2001; 30:53-57.
67. Martin DP, et al. Nonhuman primate cage modifications for environmental enrichment. Contemp Top Lab Anim Sci
2002; 41:47-49.
68. Doyle RE, Davis SD, Thomas WC. A cost-effective split level baboon condo. Lab Anim 1996; 25:49-50.
69. Coelho AM, Carey K. A social tethering system for nonhuman primates used in laboratory research. Lab Anim Sci
1990; 40:388-394.
70. Reinhardt V. Time investment for implementation of effective environment enrichment plan. Lab Primate Newsletter
1994; 33:7+.
71. Bielitzki J, et al. Improved cage design for single housing of social nonhuman primates. Lab Anim Sci 1990; 40:428-
431.
72. Anderson JH, et al. The pole and collar system: A technique for handling and training nonhuman primates. Lab Anim
1983:47-49.
73. Banerjee BN, Woodard G. A comparison of outdoor and indoor housing of rhesus monkeys (Macaca mulatta). Lab
Anim Care 1970; 20:80-82.
74. Marriott BM, Marriott RW, Jr, Norris J, et al. A semi-natural habitat for housing small nonhuman primates. J Med
Primatol 1993; 22:348-354.
75. Bryant JM. Vest and tethering system to accommodate catheters and a temperature monitor for nonhuman primates.
Lab Anim Sci 1980; 30:706-708.
76. Medicine ACoLA. Laboratory Animal Medicine & Science Series II (Version 1.0) [CD-ROM] In: Medicine ACoLA,
ed. Chester, NH: Balk, M. American College of Laboratory Animal Medicine, 2000.
77. Kelley ST, Hall AS. Housing In: Bennett BT, Abee CR,Henrickson R, eds. Nonhuman primates in biomedical research
Biology and management. San Diego: Academic Press, 1995.
78. Westergaard GC, Fragaszy DM. Effects of manipulable objects on the activity of captive capuchin monkeys (Cebus
apella). Zoo Biol 1985; 4:317-327.
79. Rosenblum LA, Andrews MW. Environmental enrichment and psychological well-being of nonhuman primates In:
Bennett BT, Abee CR,Henrickson R, eds. Nonhuman primates in biomedical research Biology and management. San
Diego, CA: Academic Press, 1995.
80. McIntyre DJ, Petto AJ. Effect of group size on behavior of group-housed female rhesus macaques (Macaca mulatta).
Lab Primate Newsletter 1993; 32:1-4.
81. Jerome CP, Szostak L. Environmental enrichment for adult, female baboons (Papio anubis). Lab Anim Sci 1987;
37:508-509.
82. Brinkman C. Toys for Boys: Environmental enrichment for singly housed adult male macaques (Macaca fascicularis).
Lab Primate Newsletter 1996; 35:5-9.
83. Animal and Plant Health Inspection Service. Final Report on Environment Enhancement to Promote the Psychological
Well-being of Nonhuman Primates. Riverdale, MD: U. S. Department of Agriculture, 1999; 1-85.
84. Animal and Plant Health Inspection Service. Draft Policy on Environment Enhancement for Nonhuman Primates.
Riverdale, MD: U. S. Department of Agriculture, 1999.
85. Seelig D. Veterinary Resources in Primatology: Primate Enrichment Forum, 1998.
86. Byron JK, Bodri MS. Environmental enrichment for laboratory marmosets. Lab Anim 2001; 30:42-48.
87. Lincoln H, III, Andrews MW, Rosenblum LA. Pigtail macaque performance on a challenging joystick task has
important implications for enrichment and anxiety within a captive environment. Lab Anim Sci 1995; 45:264-268.
88. NetVet. Environmental enrichment information resources for nonhuman primates, 1987-1992.
89. Reinhardt V, Reinhardt A, Seelig D. Environmental enrichment for nonhuman primates: An annotated bibliography for
animal care personnel: Animal Welfare Institute, 1998.
90. Animal Welfare Information Center. Bibliography on environmental enrichment, 1994.
91. Reinhardt V, Reinhardt A. Environmental enrichment for primates: An annotated database: Animal Welfare Institute,
1999.
92. Reinhardt V. Environmental enhancement for caged rhesus monkeys: A photographic documentation: Wisconsin
Primate Center, 1997.
93. Rush HG. Primate Medicine and Biology: Caging and Housing - Part II. Ann Arbor: Unit for Laboratory Animal
Medicine, University of Michigan, 2001; 1-13.
94. Bayne KAL. Nylon balls revisited. Lab Primate Newsletter 1989; 28:5 -6.
95. Bayne K. Resolving issues of psychological well-being and management of laboratory nonhuman primates. Housing,
Care and Psychological Well-Being of Captive and Laboratory Primates. New Jersey: Noyes Publications, 1989; 27-38.
96. Bayne K, et al. Influence of food enrichment on cage side preference. Lab Anim Sci 1994; 44:624-629.
97. Bayne K, Dexter S, Hurst J, et al. Kong toys for laboratory primates: Are they really an enrichment or just fomites? Lab
Anim Sci 1993; 43:78-85.
98. Bayne K, Dexter S. Results of providing swings in individually housed rhesus monkeys (Macaca mulatta). Lab Primate
Newsletter 1994; 33:9 -11.
99. Bloomsmith MA, Brent LY, Schapiro SJ. Guidelines for developing and managing an environmental enrichment
program for nonhuman primates. Lab Anim Sci 1991; 41:372 -377.
100. Boccia ML. Long-term effects of a natural foraging task on aggression and stereotypies in socially housed pigtail
macaques. Lab Primate Newsletter 1989; 28:18-19.
101. Bryant CE, Rupniak NM, Iversen SD. Effects of different environmental enrichment devices on cage stereotypies and
autoaggression in captive cynomolgus monkeys. J Med Primatol 1988; 17:257 -269.
102. Champoux M, Hempel M, Reinhardt V. Environmental enrichment with sticks for singly-caged adult rhesus monkeys.
Lab Primate Newsletter 1987; 26:5-7.
103. Chance MR, Byrne B, Jones E. A tandem cage for individually handling group-living monkeys. Lab Anim 1983;
17:129-132.
104. Clarke AS, Line SW, et al. Hormonal and behavioral responses of rhesus macaques to an environmental enrichment
apparatus. Am J Primatol 1987; 12:335 -336.
105. Comuzzie DK. Baboon vocalization as measures of psychological well-being. Lab Primate Newsletter 1993; 32:5-6.
106. Crockett D, Bielitzki J, et al. Kong toys as enrichment devices for singly -caged macaques. Lab Primate Newsletter
1989; 28:21-22.
107. Dean SW. Environmental enrichment of laboratory animals used in regulatory toxicology studies. Lab Anim 1999;
33:309-327.
108. Evans HL, et al. Methods to evaluate the well-being of laboratory primates: Comparisons of macaques and tamarins.
Lab Anim Sci 1989; 39:318-323.
109. Fajzi K, et al. A review of environmental enrichment strategies for singly caged nonhuman primates. Lab Anim 1989;
18:23-35.
110. Goosen C, Van Der Gulden W, Rozemond H, et al. Recommendations for the housing of macaque monkeys. Lab
Anim 1984; 18:99-102.
111. Heinz RD, et al. Effectiveness of enrichment devices during brief periods of social restriction in singly caged baboons.
Lab Primate Newsletter 2002; 41:1+.
112. Heinz RD, et al. Enrichment device use by baboons during long-term vs. intermittent availability. Lab Primate
Newsletter 1998; 39:1+.
113. Holmes SN, Riley JM, Juneau P, et al. Short-term evaluation of a foraging device for non-human primates. Lab Anim
1995; 29:364-369.
114. Kessel AL, Brent L, Walljasper T. Shredded paper as enrichment for infant chimpanzees. Lab Primate Newsletter
1995; 34:4-6.
115. Lehman SM, Lessnau RG. Pickle barrels as enrichment objects for rhesus macaques. Lab Anim Sci 1992; 42:392-397.
116. Lindburg DG. Ecological requirements of macaques. Lab Anim Sci 1991; 41:315-322.
117. Line SW, Houghton P. Influence of an environmental enrichment device on general behavior and appetite in rhesus
macaques. Lab Anim Sci 1987; 37:508.
118. Line SW, Markowitz H. Environmental enrichment for laboratory primates. SCAW Newsletter 1987; 9:3-5.
119. Line SW, Clarke AS, et al. Behavioral and physiologic response of rhesus macaques to an environmental enrichment
device. Lab Anim Sci 1987; 37:509.
120. Line SW, Morgan KN, Markowitz H, et al. Influence of cage size on heart rate and behavior in rhesus monkeys. Am J
Vet Res 1989; 50:1523-1526.
121. Lutz C, Farrow RA. Foraging device for singly housed longtailed macaques does not reduce stereotypies. Contemp
Top Lab Anim Sci 1996; 35:75.
122. Mendoza SP. Sociophysiology of well -being in nonhuman primates. Lab Anim Sci 1991; 41:344-349.
123. Moazed TC, Wolff AC. The raisin board as an environmental enrichment tool for laboratory primates. Lab Primate
Newsletter 1988; 27:16.
124. Murchison M. Forage feeder box for single animal cages. Lab Primate Newsletter 1996; 34:1-2.
125. Novak MA, Suomi SJ. Social interaction in nonhuman primates: An underlying theme for primate research. Lab Anim
Sci 1991; 41:308-314.
126. O'Neill P. A room with a view for captive primates: Issues, goals, related research and strategies In: Segal E, ed.
Housing, Care and Psychological Well-Being of Captive and Laboratory Primates. Park Ridge, NJ: Noyes Publications,
1989; 135-160.
127. Preilowski B, et al. Combining scientific experimentation with conventional housing: A pilot study with rhesus
monkeys. Am J Primatol 1988; 14:223-234.
128. Pyle DA, Bennett AL, Zarcone TJ, et al. Use of two food foraging devices by singly housed baboons. Lab Primate
Newsletter 1996; 35:10-15.
129. Reinhardt V, Reinhardt A. Impact of a privacy panel on the behavior of caged female rhesus monkeys living in pairs. J
Exp Anim Sci 1991; 34:55-58.
130. Reinhardt V, Smith MD. PVC pipes effectively enrich the environment of caged rhesus monkeys. Lab Primate
Newsletter 1988; 27:4 -5.
131. Reinhardt V. Preliminary comments on pairing unfamiliar adult male rhesus monkeys for the purpose of
environmental enrichment. Lab Primate Newsletter 1988; 27:1-3.
132. Reinhardt V, Cowley D, Eisele S. Serum cortisol concentrations of single -housed and isosexually pair-housed adult
rhesus macaques. J Exp Anim Sci 1991; 34:73-76.
133. Reinhardt V, Houser D, Eisele S, et al. Behavioral responses of unrelated rhesus monkey females paired for the
purpose of environmental enrichment. Am J Primatol 1988; 14:135-140.
134. Reinhardt V, Houser D, Eisele S, et al. Social enrichment of the environment of singly caged adult rhesus monkeys.
Zoo Biol 1987; 6:365-371.
135. Reinhardt V, Houser D, Eisele S. Pairing previously singly caged rhesus monkeys does not interfere with common
research protocols. Lab Anim Sci 1989; 39:73-74.
136. Reinhardt V, Houser D, et al. Preliminary comments on environmental enrichment with branches for individually
caged rhesus monkeys. Lab Primate Newsletter 1987; 26:1-3.
137. Reinhardt V. Evaluation of an inexpensive custom-made food puzzle used as a primary feeder for pair housed rhesus
macaques. Lab Primate Newsletter 1993; 32:7 -9.
138. Reinhardt V. Group formation of previously single-caged adult rhesus macaques for the purpose of environmental
enrichment. J Exp Anim Sci 1991; 34:110-115.
139. Reinhardt V, Eisele S, Houser D. Environmental enrichment program for caged macaques: A review. Lab Primate
Newsletter 1988; 27:5 -6.
140. Ross PW, Everitt JI. A nylon ball device for primate environmental enrichment. Lab Anim Sci 1988; 38:481 -483.
141. Schapiro SJ, Kessel AL. Weight gain among juvenile rhesus macaques: A comparison of enriched and control groups.
Lab Anim Sci 1993; 43:315-318.
142. Schmidt EM, Dold GM, McIntosh JS. A perch for primate squeeze cages. Lab Anim Sci 1989; 39:166 -167.
143. Seier JV, de Lange PW. A mobile cage facilitates periodic social contact and exercise for singly caged adult vervet
monkeys. J Med Primatol 1996; 25:64-68.
144. Tustin GW, Williams LE, Brady AG. Rotational use of a recreational cage for the environmental enrichment of
Japanese Macaques. Lab Primate Newsletter 1996; 35:5-7.
145. Watson DS. A built-in perch for primate squeeze cages. Lab Anim Sci 1991; 41:378-379.
146. Watson DSB, Houston BJ, Macallum GE. The use of toys for primate environmental enrichment. Lab Primate
Newsletter 1989; 28:20.
147. Taylor WJ, Laudenslager ML. Low-cost environmental enrichment plan for laboratory macaques. Lab Anim 1998;
28:28-31.
148. Williams LE, Abee CR, Barnes SR, et al. Cage design and configuration for an arboreal species of primate. Lab Anim
Sci 1988; 38:289-291.
149. Woolverton WL, Ator NA, Beardsley PM, et al. Effects of environmental conditions on the psychological well-being
of primates: A review of the literature. Life Sci 1989; 44:901-917.
150. O'Neill P. Developing effective social and environmental enrichment strategies for macaques in captive groups. Lab
Anim 1988; 17:23-36.
151. McPherson CW. Laws, Regulations, and Policies Affecting the Use of Laboratory Animals In: Fox JG, Cohen BJ,
Loew FM, eds. Laboratory Animal Medicine. Orlando, FL: Academic Press, Inc., 1984.
152. International Air Transport Association. Live Animals Regulations: IATA, 2003.
153. National Research Council. Occupational Health and Safety in the Care and Use of Nonhuman Primates In: Grossblatt
N, Vaupel S, eds. Washington, DC: The National Academies Press, 2003.
154. Hankenson FC, Johnston NA, Weigler BJ, et al. Zoonoses of occupational health importance in contemporary
laboratory animal research. Comp Med 2003; 53:579-601.

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