Wake Forest University

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Wake Forest University

• Information Regarding Nonhuman Primate Natural
  History, Behavior, Reproduction, Environmental
  Enrichment, Special Cases

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• Why is this training important?
• It serves to increase awareness of monkey
  behaviors, both threatening and non-threatening.
• It provides non-human primate handlers with a
  detailed look at the Wake Forest University Plan
  for Nonhuman Primate Environmental Enrichment.

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Lets begin with some background. . .
Important Note No images contained herein were
taken at Wake Forest University School of
Medicine unless otherwise indicated.
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Wake Forest University School of Medicines
conducts research with four Old World species of
monkeys.
The terms Old World and New World refer to
the species place of origin
Old World monkeys are native to Africa and Asia
New World monkeys are native to southern
Mexico, Central America and South America.
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• African Green monkeys (Chlorocebus ethiops)
• Also known as Vervet monkeys

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• Rhesus monkey (Macaca mulatta)

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• Cynomolgus monkey (Macaca fascicularis)
• Also called crab-eating macaque, long-tailed
  macaque, and Java monkey

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• Bonnet monkey (Macaca radiata)

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Common Physical Features

• Old World monkeys share several common physical
  features

Quadrapedal walk on all fours
Cheek pouches for food storage in the mouth
Opposable thumb enables grasping
Large canine teeth and sharp fingernails
Non-prehensile tail used for balance rather
than grasping objects or substrates
Ischial callosities - hairless, callused areas on
either side of the rump used for sitting (also
called butt pads)
Sexual dimorphism males are bigger in size than
females
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• Macaques and Vervet monkeys are omnivorousthey
  consume both plant and animal material. In fact,
  Vervet monkeys are the most omnivorous of all
  primate species. Their diet may consist of the
  following

• grasses
• fungi
• fruit
• berries

• flowers
• buds
• shoots
• invertebrates

• birds
• bird eggs
• lizards
• rodents
• other vertebrate prey

• leaves
• acacia tree gum
• seeds
• nuts

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Mating and Reproduction
Females typically begin cycling around 2.5 yrs
of age, but may begin as early as 1.5 yrs.
Early weaning can result in psychological
problems and inadequate development of social and
maternal skills.
Juveniles become sexually mature at 3 to 4 years
of age.
Females have sex skin genital areas (also
sometimes face and arms) turn red and swollen
around ovulation signals males to their
receptiveness to mating. (Note Vervet and bonnet
monkeys do not have sex skin.)
Gestation lasts between 5 6 months.
Infants are nursed between 10 and 12 months, and
weaning occurs around 12 months old.
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Question/Answer
Which of the following species ARE NOT housed at
WFUSM?
A. African Green monkeysB. ChimpanzeesC. Rhesus
monkeysD. Cynomolgus monkeys
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Monkey Behaviors
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• Macaques and vervet monkeys are both arboreal and
  terrestrial.
• Macaques and vervet monkeys are social animals
  and live in groups of multiple males and females.

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• Within groups, individuals are ranked according
  to dominance status.
• Dominance is often determined by the rank of the
  mother, which creates what is called a
  matrilineal dominance hierarchy.

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• Dominant animals benefit from having first access
  to and control over food, higher rates of
  successful breeding, social exchanges such as
  grooming, and control of other desirable
  resources (preferred perches, objects).
• Young males leave the group and form bachelor
  troops before reaching sexual maturity, while the
  females stay with their family group, often for
  life.

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Most of their communication is done through
facial signals and vocalizations. There are
several types of facial signals for communication.
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Threatening Behaviors

• Threat displays

• Open mouth threat mouth opens and forms the
  shape of an O
• Threat yawn tilting head back while opening
  mouth wide, exposing the teeth

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Threatening Behaviors

• Other Threatening Displays

A direct stareto Old World monkeys, such as
macaques and vervets, direct eye contact is a
sign of aggression
Shaking an object in the environment, such as the
cage door
Charging with the intent to fight
Raising eyebrows quickly and repeatedly
Piloerection hair stands on end
A jerky head-bob
Slapping the ground
Flapping the ears
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Friendly/Submissive Behaviors

• Grooming not only reduces fur parasite load, but
  its also important for forming and maintaining
  social bonds.
• Studies have shown that a monkeys heart rate is
  significantly lower when being groomed by another
  than when self-grooming or while displaying any
  other behaviors.

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Friendly/Submissive Behaviors

• Embracing
• Sitting in close proximity

• Lip Smacking bringing the lips together
  repeatedly and rapidly without showing the teeth,
  making a slight smacking sound

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Friendly/Submissive Behaviors

• Coo calls can be used as food calls (made upon
  discovery of a low quality food) or used to make
  auditory contact with group members.

• Food sharing has often been used as an indicator
  of a socially compatible pair of monkeys.

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Friendly/Submissive Behaviors

• Fear grimacing pulling back the lips to reveal
  the teeth while the mouth is closed
• Resembles a human smile
• Indicates fear, submission, and no intent to
  attack

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Auditory Communication

• Monkeys also rely on vocalizations to communicate
  with other monkeys.
• Vocalizations can be used to contact members of
  the group, alert others to a predator, beg for
  food, and convey emotions (aggression, fear,
  excitement).
• Vervet monkeys have evolved specific alarm call
  vocalizations to alert their group to the
  presence of different predators. Examples
• leopard alarm call
• snake alarm call
• eagle alarm call
• Vervet monkeys recognize the different alarm
  calls and will respond accordingly after hearing
  them. For example, if the snake alarm call is
  given, Vervets have been observed looking down in
  the grass to detect the predator.

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Vocalizations

• Please click on the links to listen to samples
  and to view videos
• Samples of different Rhesus vocalizations
• http//www.wjh.harvard.edu/7Emnkylab/media/rhesu
  scalls.html
• Samples of different Vervet vocalizations
• http//www.wjh.harvard.edu/7Emnkylab/media/verve
  tcalls.html

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Question/Answer
Which of the following is NOT a threatening
behavior?
A. StaringB. YawningC. Lip smackingD. Piloerect
ion
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Human-Monkey Interactions
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Interactions with Laboratory Primates
Laboratory primates are not pets. They are wild
animals and should be respected.
Because eye contact is interpreted by monkeys as
a sign of aggression, avoid staring directly into
a monkeys face.
Respect the physical space of monkeys by not
putting your hands into their caging or standing
too close to their caging.
Like humans, monkeys have comfort zones for
proximity to others.
Unsolicited touching or attempts at petting may
be interpreted as aggression and the monkey may
respond aggressively in return.
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Interactions with Laboratory Primates
If a monkey is acting fearfully or aggressively
towards a human by displaying threats,
vocalizations, or making physical contact, the
proper way to respond is to avert your gaze, step
out of reach, and IGNORE the undesirable
behaviors.
If your job requires working closely with a
monkey who is acting aggressively, ask for help
from your supervisor.
It is NEVER acceptable to attempt to punish a
monkeys inappropriate behavior by staring,
returning threats, becoming physical, or using
other measures of punishment such as the squeeze
bar or water hose.
Any overt aggression or punishment will be
subject to disciplinary action.
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Interactions with Laboratory Primates
If you ever witness inappropriate treatment of a
monkey or questionable research procedures 1.
Report it to your supervisor immediately. OR 2.
Make an anonymous report to the Animal Care and
Concern Hotline at 716-5899. OR 3. Make an
anonymous report to the Research Concern Hotline
at 716-0338.
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Question/Answer
The best way to respond to a monkey who is acting
aggressively is to
A. Stare them downB. Yell at them and slap the
cageC. Ignore the behavior and take a
time-outD. Distract them with treats
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Environmental Enrichment
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Environmental Enrichment
Question What is Environmental Enrichment?
Environmental Enrichment is defined as changes
made to the environment and husbandry practices
that provide the opportunity for choice and the
expression of species-typical behavior.
Question Why is Environmental Enrichment
important?
Congress responded to public concern for animals
used in research by passing the Animal Welfare
Act of 1966 and 1978. When the U.S. Department
of Agriculture (USDA) adopted the act as
regulations in 1991, it required that dealers,
exhibitors, and research facilities must develop,
document, and follow an appropriate plan for
environmental enhancement adequate to promote the
psychological well-being of nonhuman primates.
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Assessing Psychological Well-Being

• To assess psychological well-being, we need to
  address the following criteria
• The animals ability to cope with day-to-day
  changes in its social and physical environment
• The animals ability to engage in beneficial
  species-typical activities
• The absence of maladaptive behaviors that result
  in self-injury or negative consequences
• The presence of a balanced temperament (balance
  of aggression and passivity) and absence of
  chronic signs of distress (distress
  vocalizations, depressed postures, labored
  breathing, excessive cardiac response, lack of
  appetite, abnormal hormone concentrations)

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Environmental Enrichment Plan

• The Wake Forest University Plan for Nonhuman
  Primate Environmental Enrichment seeks to
  facilitate psychological well-being by
  implementing five major types of enrichment
• Structural enrichment
• Food enrichment
• Sensory enrichment
• Object enrichment
• Social enrichment

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Structural Enrichment

• Housing design should allow the expression of
  species-typical postures and movement.
• Cage furnishings such as perches, climbing
  structures, shelves, barrels, and tunnels have
  been used to allow monkeys to assume a variety of
  movements and postures, have access to vertical
  space, and to have some form of privacy when
  socially housed.
• Monkeys prefer to sit and sleep on perches and
  will seek out the highest point in the
  environment when threatened.
• All cages at WFU are required to be equipped with
  perches.

Examples follow . . .
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Structural Enrichment
Milk crates and surgical tubing serve as swings,
perches, and food puzzles.
Various swings made from fire hose and PVC
tubing the barrel serves as a swing, shelter,
and hiding place.
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Structural Enrichment
Wooden cable spools offer shelter, a hiding
place, and area for climbing monkeys also enjoy
gnawing wood.
WFUSM image
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Structural Enrichment

• To reduce and manage social conflict, each cage
  must be equipped so that monkeys can escape the
  aggressive displays of others. In a social
  setting, barrels make very good hiding places.
• Monkeys who are housed individually in cages
  must also have a way to avoid eye contact with
  other monkeys housed in the same room.

Visual barriers offer individually housed
monkeys the option of privacy. Visual barriers
attach to the front of the cage, where the monkey
can choose to sit behind it.
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Food Enrichment

• Monkeys in the wild typically spend about 70 of
  their time foraging for food.
• Offering primates the opportunity to engage in
  this behavior is one of the simplest and most
  important tools in ensuring psychological
  well-being and preventing abnormal behaviors.
• In the research setting, our goal is to increase
  manipulation and exploration, the time required
  to procure food items, and the time required to
  ingest food items.
• There are many commercial devices designed to
  enable foraging behavior.

Examples follow . . .
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Food Enrichment

• Some examples of foraging devices that can be
  loaded with food

Challenger ball
Kong toy
Primate Choo
PVC food puzzle
Holee Molee ball
Foraging turf board
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Food Enrichment

• In addition to devices, natural food itemscan
  provide the opportunity for foraging.
• Examples
• corn on the cob
• bird seed
• food and flavored liquids frozen in ice cube
  trays
• pomegranate
• whole coconut

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Food Enrichment

• Like human primates, monkeys enjoy a wide variety
  of foods and novel treats. There are several
  online nonhuman primate recipe resources, such as
  The Cattarhine Café Cookbook, created by
  Washington National Primate Research Center.

This recipe collection can be found online at
http//www.wanprc.org/wanprc/cookbook-forExternal.
pdf
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Question/Answer
In the wild, monkeys spend a majority of their
time engaged in which behavior
A. ReproductionB. Fighting C. GroomingD. Foragi
ng for food
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Sensory Enrichment

• In some cases, monkeys may participate in daily
  experimental sessions. This may involve
  manipulating joysticks, response levers, or
  making operant responses to obtain food pellets.
  After initial training, it is clear that such
  rewarded responses contribute to psychological
  well-being.
• Other types of sensory enrichment include
• Music and television
• Training through positive reinforcement
• Novel scents the ARP provides novel scent
  enrichment with liquid potpourri one day each
  week.
• Swimming

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Sensory Enrichment

• Macaques are skillful swimmers. Here are pictures
  of macaques enjoying a swimming pool.

Plastic Sand Box
Livestock Water Tank
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Object Enrichment

• Object enrichment includes durable, manipulable
  objects such as mirrors, plastic balls,
  cone-shaped rubber toys, and gnawing sticks that
  are safe to be used by monkeys.
• Objects should be rotated at least every two
  weeks to maintain novelty and should be
  replaced when worn or damaged.

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Social Enrichment
Monkeys are social animals. As such, living
with an animate, responsive mate is the best form
of environmental enrichment.
Group and pair housing reduces boredom and
anxiety and facilitates expression of a wider
range of species-typical behaviors.
Individually housed monkeys should be provided
increased environmental enrichment, and visual,
auditory, and olfactory contact with other
monkeys via close caging, a mesh cage divider, or
grooming panel.
Monkeys who are socially housed develop better
coping skills and are less likely to display
abnormal and self-injurious behaviors.
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Special Cases
While monkeys generally adapt well to living in
captivity, some monkeys develop abnormal and
sometimes self-injurious behaviors.

• Behaviors that may be considered abnormal are
• repetitive locomotion
• withdrawn or depressed behavior
• self-directed biting or physical aggression
• hair pulling or excessive grooming of self or
  others
• coprophagy excessive ingestion of feces
• excessive aggression

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Documenting Abnormal Behavior
Step 2 The veterinarian will conduct a
physical exam and if there are no biological
bases for the behavior of concern, the EEC will
conduct an initial assessment in concert with the
enrichment contact person designated in the
Nonhuman Primate Environmental SOP protocol.
Step 1 Any abnormal or detrimental behaviors
exhibited by a monkey should be recorded on a
daily log sheet and reported first to a
veterinary staff member and then to the
Environmental Enrichment Coordinator (EEC) within
the ARP.
Step 4 As determined by the EEC, the contact
person, and/or the consulted parties, an
enrichment regimen may be individually prescribed
and carried out by the investigators lab. The
EEC and contact person will monitor the success
or failure of the enrichment strategy and take
part in any necessary adjustments to that
strategy.
Step 3 After the assessment, the EEC will
determine whether the behaviors of concern
require an additional evaluation by a veterinary
staff member or by a behavioral primatologist and
will coordinate those evaluations.
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Question/Answer
Which of the following behaviors is considered
abnormal?
A. Depressed behaviorB. Self-directed aggression
C. Hair pulling or overgroomingD. All of the
above
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Question/Answer
Monkeys are social animals. The best form of
environmental enrichment is
A. Food enrichmentB. Structural enrichment
C. Object enrichmentD. Social enrichment
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Question/Answer
Any observations of abnormal behaviors should be
reported to
A. Your supervisorB. A veterinary staff member
C. The Environmental Enrichment Coordinator
(EEC)D. All of the above
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Contact Information
Important Contact Information Environmental
Enrichment Coordinator (EEC) 716-1506 ARP-Bowman
Gray Campus 713-7394 ARP-Friedberg
Campus 716-1620 ARP-Downtown
Campus 713-1171
Test code to follow . . .
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References

• Bayne, K. 2005. Enrichment for Nonhuman Primates
  Macaques, NIH Pub No. 05-5744. Department of
  Health and Human Services.
• Boccia ML, Reite M, Laudenslager ML 1989. On the
  physiology of grooming in a pigtail macaque.
  Physiology and Behavior 45, 667-670.
• National Research Council. 1998. The
  Psychological Well-Being of Nonhuman Primates.
  Washington, DC National Academy Press.
• National Research Council. 1996. Guide for the
  Care and Use of Laboratory Animals. Washington,
  DC National Academy Press.

Test code to follow . . .
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References

• http//pin.primate.wisc.edu/ (Primate Info Net
  Website for information and publications
  regarding primates and enrichment)
• http//www.snprc.org/macaque/faq/macaquefaq.html
  (Website for information on macaques)
• http//www.wjh.harvard.edu/7Emnkylab/media/rhesus
  calls.html (Website for samples of different
  rhesus vocalizations)
• http//www.wjh.harvard.edu/7Emnkylab/media/vervet
  calls.html (Website for samples of different
  Vervet vocalizations)
• http//www.wanprc.org/wanprc/cookbook-forExternal.
  pdf (The Catarrhine Cafe Cookbook)

Test code to follow . . .
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To receive credit

• To receive credit for this course, you must pass
  the online test. You will need to retain the
  following number in order to access the test
• The test can be accessed by closing this
  PowerPoint presentation and clicking on Take
  Course Test within the HR SelfService menu,
  Environmental Health Safety Courses and Tests.

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Thank you for your time!
Passing grade 80