enrichment
Kathryn Bayne, M.S., Ph.D., D.V.M., DACLAM, CAAB
AAALAC International
Macaques
for nonhuman primates
Macaques
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Macaques
Introduct�on
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” exhib-
its; 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-be-
ing. 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 effec-
tive, 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 so
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Macaques
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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 chap-
ter 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 Feu-
rer, editor, and Ms. Lori Wieder, graphics and layout production, for their as-
sistance 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. Spe-
cial 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 Ameri-
can 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.
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Macaques
Background
Hab�tat
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.
Phys�cal 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 aver-
age 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.
Rhesus (Macaca mulatta) monkey with cheek
pouches full of food (photo courtesy of K. Bayne).
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Macaques
Macaques
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Behav�or
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 vo-
calizations, 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-smack-
ing, and sitting in close proximity. Food sharing has also been used to assess
compatibility between pairs of animals.
Social grooming is an integral part of forming affiliations
(photo courtesy of K. Rasmussen).
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Macaques
Mat�ng and
Reproduct�on
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 ap-
proximately 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 redden-
ing 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 ma-
caque 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 defense of territory (photo courtesy of K.Rasmussen).
Macaques
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Soc�al 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 ma-
caque 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 behav-
iors, which may include
repeated pacing, circling,
or somersaulting; hy-
per-aggression; depres-
sion; and self-injurious
behavior, including hair
plucking or self-biting.
(See section on “Problem
Behaviors”).
While group or pair
housing is strongly
recommended for ma-
caques, 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 hier-
archy without support from other animals.
Evidence of hair-plucking behavior, a type of self-injurious
behavior (SIB) on the leg of this macaque
(photo courtesy of K. Bayne).
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Macaques
One approach to forming pairs of macaques is provided at the end of this chap-
ter. 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.
Offering vulnerable areas of the body to be groomed by another
animal indicates a degree of trust and affiliation between the animals
(photo courtesy of K. Bayne).
Providing three-dimensional space in the primary
enclosure, using Primahedrons®
(photo courtesy of K. Bayne).
Macaques
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Phys�cal World
Hous�ng
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 construct-
ed of materials that cannot loop around the neck, such as flexible polyvinyl chlo-
ride (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 cap-
tive 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 swim-
ming 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.
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A horse water trough, shown here, serves as a swimming
pool for young macaques (photo courtesy of K. Bayne).
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Macaques
Enr�chment
The macaques are curious and intelligent animals. Providing them with op-
portunities 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 be-
come 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.
Flexible PVC tubing
can be installed in the
primary enclosure to
simulate branches for
swinging (photo courtesy
of K. Bayne).
A variety of toys used with
macaques (photo courtesy of K.
Bayne and S. Dexter).
The damage inflicted on toys after usage
by macaques. Small remnants can pose
a choke hazard to the animals (photo
courtesy of K. Bayne and S. Dexter).
Macaques
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A very successful way to fulfill these ani-
mals’ 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, offer-
ing captive primates the opportunity to
engage in this behavior can be important
in preventing the development of abnor-
mal behaviors. Numerous in-house and
commercially produced devices are avail-
able, 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 search-
ing 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.
Food treats may be dispensed from
puzzle balls (photo courtesy of K. Bayne
and S. Dexter).
Wedging food treats inside a Kong® toy is another
way to extend the animal’s time spent in “foraging”
(photo courtesy of W. Brandon).
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Macaques
This animal forages
for food “crumbles” in
an artificial shearling
foraging/grooming board
(photo courtesy of K.
Bayne).
Spec�al Cases
Age-related Cons�derat�ons
The macaques are long-lived animals, with reports of some animals living in
captivity over 30 years. This lifespan entails a commitment of considerable dura-
tion, 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 ar-
thritis, 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.
Ind�v�dual Hous�ng
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
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Macaques
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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.
Suscept�b�l�ty to D�sease
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