Back
to Table of ContentsBibliography on Refinement and Environmental Enrichment for Primates. Enrichment 1-3
(6) Promoting Object-oriented Behavior
(7) Promoting Curiosity
Behavior (watching videos; watching out of the window)
(8) Safety Concerns
Environmental enrichment provides more species-adequate living and handling conditions thereby buffering stress and distress responses to captivity.Environmental enrichment is the provision of stimuli which promote the expression of species-appropriate behavioral and mental activities in an understimulating artificial environment.
United States Department of Agriculture
1991. Title
9, CFR (Code of Federal Register), Part 3. Animal Welfare; Standards;
Final Rule. Federal Register 56(No. 32), 6426-6505
"The physical environment in the primary enclosures must
be enriched by providing means of expressing noninjurious species-typical
activities. .. Examples of environmental enrichment include providing
perches, swings, mirrors, and other increased cage complexities;
providing objects to manipulate; varied food items; using foraging
or task-oriented feeding methods; and providing interaction with
the care giver or other familiar and knowledgeable person consistent
with personnel safety precautions."
Canadian Council on Animal Care, Olfert
ED, Cross BM, McWilliam AA 1993. Guide
to the Care and Use of Experimental Animals, Volume 1, 2nd
Edition. Canadian Council on Animal Care, Ottawa
"The social needs of animals used in research, teaching,
or testing, should be given equal consideration with environmental
factors such as lighting, heating, ventilations and containment
(caging). Particularly in the case of singly housed animals, daily
observation provides an alternative from of social contact for
the animal and commonly facilitates handling in that the animal
becomes accustomed to the human presence. .. Most animals should
not be housed singly unless required by medical condition, aggression,
or dictates of the study. Singly housed animals should have some
degree of social contact with others of their own kind. ... In
the interest of well-being, a social environment is desired for
each animal which will allow basic social contacts and positive
social relationships. Social behaviour assists animals to cope
with circumstances of confinement."
European Commission
2002. The Welfare of Non-human Primates - Report of the Scientific
Committe on Animal Health and Animal Welfare. European Commission,
Strasbourg, France
http://europa.eu.int/comm/food/fs/sc/scah/out83_en.pdf
"Primates should not be housed singly unless fully justified
by health considerations (for the animal and human handler) or
research procedures, as advised following an ethical review process.
If primates have to be singly housed, the animals should have
visual, olfactory and autitory contact with conspecifics.”
European Economic Community 1986.
Council Directive 86/609 on the Approximation of Laws, Regulations,
and Administrative Provisions Regarding the Protection of Animals
Used for Experimental and Other Scientific Purposes, Annex II
Guidelines
for Accommodation and Care of Animals. Official Journal
of the European Communities L358 , 7-28
European guidelines for housing and handling of laboratory
animals. "The performance of an animal during an experiment
depends very much on its confidence in man, something which has
to be developed. ... It is therefore recommended that frequent
contact should be maintained so that the animals become familiar
with human presence and activity. Where appropriate, time should
be set aside for talking, handling and grooming. The staff should
be sympathetic, gentle and firm when associating with the animals."
International Primatological Society
1993. IPS
International guidelines for the acquisition, care and breeding
of nonhuman primates, Codes of Practice 1-3. Primate Report
35, 3-29
" A compatible conspecific probably provides more appropriate
stimulation to a captive primate than any other potential environmental
enrichment factor. ... Monkeys should, unless there are compelling
reasons for not doing so, be housed socially. ... Young monkey
should not normally be separated from its mother at an early age
(i.e., at 3-6 months) but should remain in contact for one year
to 18 months, in most species. There is unlikely to be any greater
productivity through early weaning, in seasonally breeding species,
such as rhesus monkeys. Even in non-seasonal breeders, any slight
increase in productivity must be offset against the resulting
behavioural abnormalities of the offspring."
National Research Council 1996. Guide for the
Care and Use of Laboratory Animals, 7th Edition. National
Academy Press, Washington
"Animals should be housed with the goal of maximizing
species-specific behaviors and minimizing stress-induced behaviors.
For social species, this normally requires housing in compatible
pairs or groups."
National Research Council 1998. The
Psychological Well-Being of Nonhuman Primates. National
Academy Press, Washington
"Social interactions are considered to be one of the most
important factors influencing the psychological well-being of
most nonhuman primates. ... The common practice of housing rhesus
monkeys singly calls for special attention [p. 99] ... Every effort
should be made to house these [singly caged] animals socially
(in groups or pairs), but when this is not possible, the need
for single housing should be documented by investigators and approved
by the IACUC. ... The animal technician's and caregiver's roles
are pivotal to the social support of primates, particularly animals
that are singly caged."
United States Department of Agriculture
1991. Title
9, CFR (Code of Federal Register), Part 3. Animal Welfare; Standards;
Final Rule. Federal Register 56(No. 32), 6426-6505
The environmental enhancement plan "must include specific
provisions to address the social needs of nonhuman primates of
species known to exist in social groups in nature. ... Examples
of environmental enrichment include ... providing interaction
with the care giver or other familiar and knowledgeable person
consistent with personnel safety precautions."
(2,1,a) Group-housing: Practical Issues
Alford PL, Bloomsmith MA, Keeling
ME, Beck TF 1995. Wounding aggression during the formation and
maintenance of captive, multimale chimpanzee groups. Zoo Biology
14, 347-359
"There is more wounding and more severe wounding in groups
composed of older, socially experienced males than in groups composed
of younger socially inexperienced males, many of whom also had
extensive visual exposure to one another before grouping."
Baker KC, Seres M, Aureli F, de Waal
FBM 2000. Injury risks among chimpanzees in three housing conditions.
American Journal of Primatology 51, 161-175
"Over a two-year period all visible injuries to 46 adult
males, 64 adult females, and 25 immature chimpanzees were recorded.
... Housing included compounds containing about 20 chimpanzees,
interconnected indoor-outdoor runs for groups of up to 12 individuals,
and smaller indoor-outdoor runs for pairs and trios. ... Compound-housed
chimpanzees incurred the highest level of minor wounding, but
serious wounding levels were not affected by housing condition.
... Overall, this study indicates that maintaining chimpanzees
in pairs and trios would not be an effective means for reducing
injuries. The management of wounding in chimpanzee colonies is
influenced more by the sex and rearing composition of a colony."
Bellinger LL, Hill EG, Wiggs RB 1992.
Inexpensive modifications to nonhuman primate cages that allow
social grouping. Contemporary Topics in Laboratory Animal Science
31(3), 10-12
"These two design modifications [PVC tunnels and stainless
steel tunnels connecting two adjacent cages] allow us to inexpensively
modify existing caging to meet the USDA regulations of social
grouping."
Bernstein IS 1989. Breeding colonies
and psychological well-being. American Journal of Primatology
19(Supplement 1), 31-36
Valuable discussion of relatively safe group-housing management
practices.
Bloomsmith MA 1989. Interaction between
adult male and immature captive chimpanzees: Implications for
housing chimpanzees. American Journal of Primatology 19(Supplement
1), 93-99
"These observations suggest that captive adult male chimpanzees
have the potential to develop affiliative relationships with immature
conspecifics. Housing adult males in groups along with infants
may be an important way of increasing the social complexity of
the males' environments."
Boyce WT, O'Neill-Wagner PL, Price
CS, Haines MC, Suomi SJ 1998. Crowding stress and violent injuries
among behaviorally inhibited rhesus macaques. Health Psychology
17, 285-289
Rhesus group of 36 animals was kept during 6 'warm' months
in a large outdoor enclosure, during 6 'cold' months confined
in a building. "During the 6-month period of confinement
stress, a fivefold acceleration in [medically-attended] injury
incidence was found."
Catlow G, Ryan PM, Young RJ 1998.
Please don't touch, we're being enriched! In Proceedings of
the Third International Conference on Environmental Enrichment
Hare VJ, Worley E (eds), 209-217. The Shape of Enrichment, San
Diego
"Enrichment often involves manipulation of animals' lives.
However, non-interference in their social lives is an important
form of environmental enrichment for chimpanzees." Rather
than locking the chimpanzees "into their indoor cages every
evening, an average of 17 hours a day" the animals were given
"continuous access to their whole area and each other 24
hours a day, except for routine cleaning. ... Almost from the
beginning [1991] the group changed. There appeared to be a calming
effect with the group actually being unified. The males became
more tolerant towards one another, and started to socialise as
a unit. ... Far more normal behaviours are present and the afternoon
tension for both animal and keeper has ceased."
Caws C, Aureli F 2001. Coping
with short-tem space restriction in chimpanzees. Primate
Eye 74, 9
"During the indoor period the chimpanzees showed no increase
in aggression, grooming, and submissive greeting, nor changed
their proximity to adult males. However, the percentage of aggressive
events that involved more than 2 individuals was significantly
lower during the indoor period. In addition, 36 dyads were identified
as "highly aggressive" during the control period; aggression
was reduced in these dyads during the indoor period. These results
confirm previous evidence that chimpanzees do not increase aggression
during space restriction. Furthermore, they seem to inhibit aggression
by not joining ongoing conflicts and by selectively decreasing
the targeting of common `victims'."
Dazey J, Kuyk K, Oswald M, Marenson
J, Erwin J 1977. Effects of group composition on agonistic behavior
of captive pigtailed macaques (Macaca nemestrina). American
Journal of Physical Anthropology 46, 73-76
Females showed significantly less aggression in the presence
of adult males [one male per group] than they did in female-only
groups.
Elton RH 1979. Baboon behavior under
crowded conditions. In Captivity and Behavior Erwin J,
Maple T, Mitchell G (ed), 125-139. Van Nostrand Reinhold, New
York
Crowding produced sharp increases in aggression, noticeable
increase in tension and general activity. "Social disintegration
[e.g., vicious aggression, social withdrawal accompanied by self-directed
behaviors], as well as individual pathology [e.g., "pulling
of hair out of other animals (by the handful) and eating it";
chewing fingers], was the end result of the crowding in this group
of baboons."
Erwin J 1977. Factors influencing
aggressive behavior and risk of trauma in the pigtail macaque
(Macaca nemestrina). Laboratory Animal Science 27,
541-547
"Provision of cover reduced aggression among members of
stable groups."
Erwin J 1979. Aggression in captive
macaques: Interaction of social and spacial factors. In Captivity
and Behavior Erwin J, Maple T, Mitchell G (eds), 139-171.
Van Nostrand, New York
Providing a male-dominated group access to two rooms rather
than one allowed some animals to be out of the dominant male's
sight. Loss of the male's control over his group resulted in a
dramatic increase in aggression among the females.
Ha JC, Robinette RL, Sackett GP 1999.
Social housing and pregnancy outcome in captive pigtailed macaques.
American Journal of Primatology 47, 153-163
"A greater number of moves decreased the probability of
a viable birth and increased gestation length and the need for
clinical treatment of the dam, while increased group size decreased
gestation length. Increased moves and group size may increase
stress by continuously shuffling social relationships, keeping
females from establishing social hierarchies, and reducing group
stability. Low group stability may increase aggression by making
females more likely to attack other females without knowing the
opponent's social position or physical abilities."
Hartner MK, Hall J, Penderhest J,
Clark LP 2001. Group-housing subadult male cynomolgus macaques
in a pharmaceutical environment. Lab Animal 30(8), 53-57
A carefully designed, successful group-formation and group-housing
protocol of five 3.5 + years old previously single-caged
cynos is described in detail. "Not only can the social complexity
of the animals' interactions be increased, but also routine tasks
can be accomplished with ease. The animals are easy to handle,
restrain, and chair train, and they readily accept biomedical
research project requirements. ... Through the maintenance of
touch gates and constant visual contact during the study [requiring
single-housing for over a month], we were able to regroup the
animals [without accidents] within 24 hours. .. Since we began
the program, the animals have transitioned through puberty and
subadult stages .. and are now cohabitating as adults."
Judge PG, de Waal BM, Paul KS, Gordon
TP 1994. Removal of a trauma-inflicting alpha matriline from a
group of rhesus macaques to control severe wounding. Laboratory
Animal Science 44, 344-350
"Results identify an unusual outbreak of serious wounding
by the alpha matriline of a large captive group [of rhesus macaques]
and indicate that identification and removal of the animals responsible
can be an effective management procedure for controlling such
injuries."
Judge P, Griffaton N, Fincke A 2001.
No effect of acute crowding on the behavior
of hamadryas baboons (Papio hamadryas). American Journal of Primatology 54(Supplement
1), 68-69
Aggressive, submissive, affiliative and self-directed responses
of the six adults - two males and four females - were recorded
in their small indoor quarters versus large outdoor section of
their enclosure. Agonistic behavior, and "scratching, an
indicator of anxiety in primates, did not increase during crowding.
.. Perhaps male hamadryas baboons exert such a controlling influence
that conflict management among the other group members is unnecessary
during crowding."
Kaplan JR, Manning P, Zucker E 1980.
Reduction of mortality due to fighting in a colony of rhesus monkeys
(Macaca mulatta). Laboratory Animal Science 30,
565-570
"Mortality resulting from fighting [17 deaths per 100
females per year] in a breeding colony of rhesus monkeys living
in groups was an important management problem. It was found that
the cause of the fighting was the social disruption resulting
from a breeding protocol which required the regular removal of
pregnant animals from groups and introduction of nonpregnant females."
Maninger N, Kim JH, Ruppenthal GC
1998. The presence of visual barriers decreases agonism in group
housed pigtail macaques (Macaca nemestrina). American
Journal of Primatology 45, 193-194
"Instances of bite, grab and chase were found to be significantly
greater [among members of harem groups of 23 pig-tailed macaques]
when visual barriers were absent compared to when they were present."
O'Neill-Wagner PL 1996. Facilitating
social harmony in a primate group. American Zoo and Aquarium
Association (AZA) Regional Conference Proceedings, 323-325
"Installing an inexpensive electric net fencing system
offered safe and innovative separation to two groups of monkeys
in the field enclosure. Animals with incentive to transfer between
areas successfully penetrated the electric net fence by leaping
over it, or darting through the mesh openings at the risk of being
zapped by a pulsating (high voltage, low amperage) electric shock.
This challenging, yet penetrable fence was functional to monkeys
in the following ways. The socially evicted males were able to
leave their natal group when the time was approaching. When responses
by animals on the other side of the fence indicated that it was
safe to return, they would do so. This system functions in a positive
way by providing evidence of tension between and within groups,
offering escape routes during aggressive interactions, [and] reducing
the potential for injuries."
Porton I, White M 1996. Managing an
all-male group of gorillas: Eight years of experience at the St.
Louis Zoological Park. American Zoo and Aquarium Association
(AZA) Regional Conference Proceedings, 720-728
"Our experience suggests that a gorilla bachelor group
is a viable and indeed a desirable alternative to solitary housing
of 'emigrated' captive males."
Reinhardt V, Reinhardt A, Houser WD
1986. Hair
pulling-and-eating in captive rhesus monkeys. Folia Primatologica
47, 158-164
It was concluded that hair pulling and eating is an aggressive
behavioral disorder reflecting adjustment problems to a stressful
[group-housing] environment.
Reinhardt V, Reinhardt A, Eisele S,
Houser WD, Wolf J 1987. Control of excessive aggressive disturbance
in a heterogeneous troop of rhesus monkeys. Applied Animal
Behaviour Science 18, 371-377
"Chronic harassment in a troop of rhesus monkeys was related
to two animals. The carefully supervised removal of these individuals
brought harmony back into the group."
Reinhardt V 1990. Catching Individual
Rhesus Monkeys Living in Captive Groups (Videotape). Available
on loan from Animal Care Audio-Visual Materials, WRPRC, 1220 Capitol
Court, Madison, WI 53715
A simple capture-chute design is demonstrated. Using vocal
commands, a single person swiftly catches all members of a trained
rhesus breeding group one-by-one in a transport box without causing
any disturbance.
Reinhardt V 1993. Nonspecific
diarrhea in the alpha-male of a breeding troop: A case report.
Laboratory Primate Newsletter 32(1), 4
"Bob's prompt recovery from intractable diarrhea upon
being removed from his troop suggests that asserting his role
as alpha-animal constituted a chronic social challenge that may
have altered his resistance to facultative pathogens and/or autonomic
neural tone, to produce diarrhea."
Rolland RM 1991. A prescription for
psychological well-being. In Through the Looking Glass. Issues
of Psychological Well-being in Captive Nonhuman Primates Novak
MA, Petto AJ (eds), 129-134. American Psychological Association,
Washington DC
"By far the most common physical problem that I treat
as clinical veterinarian is trauma sustained by macaques in group-housing
situations."
White G, Hill W, Speigel G, Valentine
B, Weigant J, Wallis J 2000. Conversion of canine runs to group
social housing for juvenile baboons. AALAS 51st National Meeting
Official Program, 126
"Our Division recently converted two rooms equipped with
10 stainless steel, elevated floor canine runs into rooms providing
social housing for young baboons. The detachable walls were removed
to create larger primary enclosures and tops were fitted with
stainless steel panels to provide complete containment. ... Our
group has trained the juvenile baboons [6 months to two years
of age] to enter squeeze cages through guillotine openings available
in the front door of the primary enclosures."
Wolfensohn S, Peters A 2005. Refinement
of neuroscience procedures using non human primates. Animal
Technology and Welfare 4, 49-50
It is demonstrated that long-tailed macaques with cranial implants
can be group-housed without undue risk. "Contrary to initial
expectations we have not found any increased incidence in infection
due to the presence of other animals or foraging substrate."
(2,1,b) Group-housing: Group Formation/Introduction/Integration
Baboons (Papio spp.)
Else JG, Tarara R, Suleman MA, Eley
RM 1986. Enclosure design and reproductive success of baboons
used for reproductive research in Kenya. Laboratory Animal
Science 36, 168-172
"The [75] females were introduced first to the cage and
given an opportunity to stabilize. The [6] males, whose canine
teeth had been cut, were paired for at least one week prior to
placement with females. Eight animals were removed within the
first month due to fight wounds and general incompatibility."
Wallis J, Hartley D 2001. Comparing two methods of forming large social
groups of captive baboons (Papio spp.). American Journal of Primatology 54(Supplement
1), 54-55
The formation of a large group of previously singly caged baboons
[unspecified sex] was most successfully accomplished gradually,
by first allowing individuals to live in small groups.
Capuchin monkeys (Cebus apella)
Bayne K, Dexter SL, Suomi SJ 1991.
Social housing ameliorates behavioral pathology
in Cebus apella. Laboratory
Primate Newsletter 30(2), 9-12
No serious aggression was associated with group formation of
two females and four males.
Cooper MA, Thompson RK, Bernstein
IS, de Waal FBM 1997. The integration of stranger males into a
group of tufted capuchin monkeys (Cebus apella). American
Journal of Primatology 42, 10
"The introductions were noteworthy for their early lack
of both aggression and affiliation. Unlike the macaque model,
in which aggression occurs immediately and relationships are settled
quickly, the social integration of male capuchins was a gradual
process."
Fragaszy D, Baer J, Adams-Curtis L
1994. Introduction and integration of strangers into captive groups
of tufted capuchins (Cebus apella). International Journal
of Primatology 15, 399-420
"Two to four unfamiliar animals were housed together for
3-5 days in one room of each resident group's two-room cage, while
the resident group remained in the other room. Following the acclimation
period, we permitted the resident group to mix with the newcomers
in the full cage. No morbidity from aggression occurred at the
time of introductions or during several months following. Introductions
of adult females can be carried out with acceptable risk to the
newcomers provided that careful monitoring occurs, so that the
onset of severe aggression instigated by resident females toward
new females can be avoided [by temporarily dividing the group
for a few days]; juveniles can be introduced with minimal risk,
and adult males can be introduced into groups lacking resident
adult males with minimal risk."
Wolff A, Ruppert G 1991. A practical
assessment of a non-human primate exercise program. Lab Animal
20(2), 36-39
Five females and three males were transferred once a week to
an exercise pen for several hours. Aggressive interactions were
never observed throughout a 9-week study period.
Chimpanzees (Pan spp.)
Bloomsmith MA, Lambeth SP 1996. Managing
aggression in multi-male, multi-female chimpanzee groups. American
Zoo and Aquarium Association (AZA) Regional Conference Proceedings,
449-452
"We found that wounding aggression was minimal during
introductions of females to males or other females, and during
male-male introductions of formerly single-caged adolescent and
young adult males having long-term prior visual familiarity. Serious
wounding occurred during male-male introductions, particularly
when there were major discrepancies in their ages and social experience."
Bloomsmith MA, Baker KC, Ross SK,
Lambeth SP 1998. Enlarging chimpanzee social groups: The behavioral
course of introductions. American Journal of Primatology
45, 171
New group members were first introduced behind mesh fencing.
Subsequent full physical contact did not further increase agonism.
All 42 introductions of chimpanzees in already established groups
were successful.
Fritz J, Howell S 2001. Captive chimpanzee
social group formation. In Special Topics in Primatology Volume
2 - The Care and Management of Captive Chimpanzees Brent L
(ed.), 172-203. The American Society of Primatologists, San Antonio
"Forming new social groups of captive chimpanzees requires
appropriate facilities, a knowledgeable staff, planning, and careful
observations." A well-tested socialization system is reviewed
which "includes a gradual acclimation of unfamiliar chimpanzees
and introductions in a controlled setting. The process has been
used to form hundreds of different social groups without serious
injuries.... Most of our 35 males live in one of seven all-male
groups. While there is considerable potential for male-male aggression
among adults, we have found males to be quite social and, in most
cases, able to live compatibly with other males. We developed
this social group strategy to provide males with increased opportunities
to form strong social bonds with other males as is common among
wild chimpanzees and as a management technique to prevent pregnancy."
The authors share extremely valuable first-hand experiences and
outline practical recommendations for the careful establishment
of new social units without undue risk of stress, distress and
injury.
Hartner MK, Hall J, Penderhest J,
Clark LP 2001. Group-housing subadult male cynomolgus macaques
in a pharmaceutical environment. Lab Animal 30(8), 53-57
A carefully designed, successful group-formation protocol of
five 3.5 + years old previously single-caged male
long-tailed macaques is described in detail.
McDonald S 1994. The Detroit Zoo Chimpanzees
Pan troglodytes: exhibit design, group composition and
the process of group formation. International Zoo Yearbook
33, 235-247
"All adults were introduced to each other first through
mesh and then physically. Before all physical introductions, the
chimpanzees involved were fed double their normal morning rations
and then fed a single ration ten minutes prior to the start of
the introduction. Play items were scattered throughout the day
room. These strategies were employed in an attempt to reduce tension
further and provide distractions. Following the dyadic/triadic
introductions, an adult female group was formed and the [two]
males were added later. All 11 Chimpanzees were successfully integrated
into one social group. The mesh and physical introductions only
produced five visible wounds, all minor and not requiring veterinary
attention."
McNary JK 1992. Integration of chimpanzees
(Pan troglodytes) in captivity. In The Care and Management
of Chimpanzees (Pan troglodytes) in captive environments
Fulk R, Garland C (eds), 88-100. North Carolina Zool Society
Clear recommendation of how to introduce new chimpanzees to
a core group and how to form a new group.
Pazol K, McDonald S, Baker K, Smuts
B 1998. Placing hand-reared chimpanzees (Pan troglodytes)
into adult social groups: A technique for facilitating group integration. Laboratory Primate Newsletter 37(3),
11-13
"This study suggests that prior housing with socially
experienced adult females can facilitate the integration of hand-reared
infants into naturalistic social groups."
Gorillas (Gorilla spp.)
Catlow G 1990. Introducing Killa-Killa.
Gorilla Gazette 4(1), 8-10
The successful introduction procedure of an adult female to
a group of two adult females and one adult male gorilla is described
in detail.
Chatfield JJ 1990. Notes on the introduction
of an aggressive male gorilla at the Los Angeles Zoo. Proceedings:
Columbus Zoo Gorilla Workshop, 2-4
The integration of a conspicuously aggressive adult gorilla
into an established group of young animals plus one adult female
is described. "The introduction took close to two years and
lots of patience and effort. The end result proved that is was
all worthwhile and certainly the risks [bite wound inflicted on
the adult female requiring surgery] were justified." The
male was tolerant toward the young animals.
Downman M 1998. The
formation of a bachelor group of gorillas at Loro Parque.
Int Zoo News 45, 208-211
Successful bachelor group formation protocol is described.
Enciso AE, Calcagno JM, Gold KC 1999.
Social interactions between captive adult male and infant lowland
gorillas: Implications regarding kin selection and zoo management.
Zoo Biology 18, 53-62
"Infants may be introduced into non-natal groups without
being attacked or physically harmed by dominant males, but their
subsequent relationships with these males may lack the close,
affiliative interactions that enhance infant social development."
Jendry C 1989. Gorilla introductions.
Gorilla Gazette 3(3), 5-6
A well-tested introduction protocol is outlined step-by-step.
Johnstone-Scott R 1992. The
integration of Julia. International Zoo News 39(6),
18-26
Successful integration procedure of an adult female gorilla
into an established breeding group is described.
McCann CM, Rothman JM 1999. Changes
in nearest-neighbor association in a captive group of Western
Lowland gorillas after the introduction of five hand-reared infants.
Zoo Biology 18, 261-278
The integration of five hand-reared infants into a group of
5 females and 1 male was successful and without incident. "Findings
lend strong support to the importance of peer groups [security/companionship]
and the presence of a silverback male for facilitating the integration
of hand-reared infants into established groups."
Meder A 1985. Integration of hand-reared
gorilla infants in a group. Zoo Biology 4, 1-12
Zoo-born gorilla infants "could best be introduced into
a group when about 1.5 to 2 years old; when younger or older,
social integration becomes more difficult. An introduction to
adult females in a small cage until strong social relations are
formed leads to a smoother social integration in the whole group
afterward and takes less time than socializing the infants to
juveniles. Allowing the infants to explore the group's main enclosure
alone and before they join the group permanently leads to better
spacial orientation for them and helps to lessen their uneasiness
in the new social situation. Providing the infants with a shelter
within the group's enclosure, which gives them access to the group
but is inaccessible to the adults, reduces tension and thus aggression
toward them."
Winslow S, Ogden J. J., Maple TL 1990.
Socialization of an adult male lowland gorilla (Gorilla gorilla
gorilla). Proceedings: Columbus Zoo Gorilla Workshop
, 195-204
Successful group formation process of an adult male, an adult
female, and a juvenile female is outlined.
Macaques (Macaca spp.)
Asvestas C, Reininger M 1999. Forming a bachelor group of long-tailed macaques
(Macaca fascicularis).
Laboratory Primate Newsletter 38(3), 14
The careful establishment of a compatible group of 24 male
long-tailed macaques is described. "The worst injuries were
a split lip and a bite to the leg, both of which healed up quickly."
Bernstein IS, Gordon TP 1977. Behavioral
research in breeding colonies of Old World monkeys. Laboratory
Animal Science 27, 532-540
"In our experience, the simultaneous release of all animals
has proven to produce the fewest injuries and the most rapid social
integration. The addition of individuals to such a colony results
in the mobbing of adults, often with severe consequences. Once
a group is established, one should avoid adding animals no matter
how desirable this might appear. If new groups are to be established,
it is far less damaging to the stability of the colony to divide
a group along matrilineal lines than to remove any particular
age class."
Clarke AS, Czekala NM, Lindburg DG
1995. Behavioral and adrenocortical responses of male cynomolgus
and lion-tailed macaques to social stimulation and group formation.
Primates 36, 41-46
"Males were exposed to a mirror, then visually exposed
to conspecific neighbors in all pairwise combinations, and then
formed into conspecific groups [of 3 animals each]. Following
group formation [urinary] cortisol values showed a decreasing
trend in the cynomolgus, but not in the lion-tails. The cynomolgus
rapidly adapted to group living and relations between them were
primarily affiliative. In contrast, no affiliative behavior was
ever observed in the lion-tail group, which appeared to be highly
stressed by group living and was eventually disbanded."
Clarke MR, Blanchard JL 1994. All-male
social group formation: Does cutting canine teeth promote social
integration? Laboratory Primate Newsletter 33(2), 5-8
Groups of rhesus males were formed by releasing future group members
in same enclosure. Within the first five months after group formation
one of 26 animals died and two were killed due to trauma resulting
from fighting.
Good GP, Sassenrath EN 1980. Persistent
adrenocortical activation in female rhesus monkeys after new breeding
group formation. Journal of Medical Primatology 9, 325-334
"Persistent elevated adrenocortical responsiveness to
ACTH has been demonstrated in female rhesus monkeys as long as
13 weeks after relocation into new single male breeding groups."
Gust DA, Gordon TP, Wilson ME, Brodie
AR, Ahmed-Ansari A, McClure HM 1991. Formation of a new social
group of unfamiliar female rhesus monkeys affects the immune and
pituitary adrenocortical systems. Brain, Behavior, and Immunity
5, 296-307
Eight females were introduced into an enclosure. "Dominance
rank was established within 48 h by noncontact threats and chases
and was unchanged throughout the study. Only two minor wounds
were recorded." The animals showed physiological stress responses
during the first 9 weeks after group formation.
Jensen GD, Blanton FL, Gribble DH
1980. Older monkeys' (Macaca radiata) response to new group
formation: Behavior, reproduction and mortality. Experimental
Gerontology 15, 399-406
"A group of younger bonnets (5 males and 33 females under
10 yrs of age) suffered 11% mortality in the first three months
after new group formation, the death all due to trauma."
Kessler MJ, London WT, Rawlins RG,
Gonzales J, Martines HS, Sanches J 1985. Management of a harem
breeding colony of rhesus monkeys to reduce trauma-related morbidity
and mortality. Journal of Medical Primatology 13, 91-98
Mortality rates per year were reduced from 13.4% to 3.5% "when
monkeys were maintained in permanent harems to which returning
females were reintroduced compared to new social groups formed
from aggregates of unfamiliar animals."
Line SW, Morgan KN, Roberts JA, Markowitz
H 1990. Preliminary
comments on resocialization of aged macaques. Laboratory
Primate Newsletter 29(1), 8-12
Each rhesus monkey [6 males and 7 females] was introduced to
group members in a series of brief pair tests. The incidence of
serious injury was 62% including one fatality.
Meshik VA 1994. Group
formation in adult Japanese macaques. International Zoo
News 41(3), 5-9
"Starting with submissive animals, individuals from the
first group [2 females and 1 male] were introduced step by step
to the second [resident] group [3 females and 1 male]. A new group
was successfully formed without severe fighting. There were practically
no aggressive acts."
Reinhardt V 1991. Group
formation of previously single-caged adult rhesus macaques for
the purpose of environmental enrichment. Journal of Experimental
Animal Science 34, 110-115
"Future group members [of the same sex, 6 females and
6 males] were given ample opportunity to physically interact with
each other on a one-to-one basis and were considered ready for
group formation only when they had demonstrated compatibility
and clear-cut dominance-subordination relationships." Persistent
aggressive interactions made it imperative to disband both groups
shortly after group formation.
Rhine RJ, Cox RL 1989 How not to enlarge
a stable group of stumptailed macaques (Macaca arctoides).
In Housing, Care and Psychological Well-being of Captive and
Laboratory Primates Segal EF (ed), 255-269. Noyes Publications,
Park Ridge
"The best advice, based on our experience with established
groups of stumptails, is to combine groups, or introduce adult
animals, only as a very last resort, and then with great care
and assiduous monitoring."
Schapiro SJ, Lee-Parritz DE, Taylor
LL, Watson L, Bloomsmith MA, Petto AJ 1994. Behavioral management
of specific pathogen-free rhesus macaques: Group formation, reproduction,
and parental competence. Laboratory Animal Science 44,
229-234
Initial group formation was amicable. "However, during
the first breeding season, there were outbreaks of severe aggression,
leading to the permanent removal of three [of seven] males and
17 [of 50] females."
Stahl D, Herrmann F, Kaumanns W 2001.
Group formation of a captive all-male group
of lion-tailed macaques (Macaca silenus). Primate Report 59, 93-108
"The [6 adult (5 years and older)] individuals were brought
together simultaneously. .. .. The individuals showed no fights
or other serious aggression during the first encounter on the
first day. Aggression rates were high only during the first hour
after introduction of the animals. Afterwards, the aggression
level remained within a similar low level during the whole observation
period. .. The development of the social relationships within
the first days suggests that there is a certain degree of social
compatibility between male lion-tailed macaques.. .. After four
days, the zoo decided to remove Heiner from the group. The animal
did not show conspicious aggressive behaviour but it was thought
that he was not compatible with the other animals in the group.
Four weeks after the group establishment Nepomuk died because
of a chronic, subacute gastritis. Two months later, another monkey,
Smokie, died because of a bacterial infection. To prevent further
risks the group was disbanded at the end of December 1995."
Westergaard GC, Izard MK, Drake JD,
Suomi SJ, Higley JD 1999. Rhesus macaque (Macaca mulatta)
group formation and housing: Wounding and reproduction in a specific
pathogen free (SPF) colony. American Journal of Primatology
49, 339-347
Initially small groups were formed consisting of one male and
up to eight females. Subsequently larger groups [about 3 males
and 21 females] were formed by releasing group members simultaneously
or incrementally" When forming rhesus macaque breeding groups
from partial groups and strangers, a staged group formation method
leads to lower traumatic wounding rates than does a rapid formation
method in which all individuals are put together at once. When
forming new rhesus macaque breeding groups, divided corrals that
provide for social and visual separation of individuals lead to
lower rates of traumatic wounding than do undivided corrals."
Orangutans (Pongo pygmaeus)
Hamburger L 1988. Introduction of
two young orangutans, Pongo pygmaeus, into an established
family group. International Zoo Yearbook 27, 273-278
Successful re-introduction of two hand reared young orangutans
into a family group is described.
Watts E 1997. Introductions. In Orangutan
Species Survival Plan Husbandry Manual Sodaro C (ed), 69-84.
Atlanta Orangutan SSP [Species Survival Plan], Atlanta
Group integration and re-introduction techniques are described
and very valuable recommendations made.
Squirrel monkeys (Saimiri spp.)
King JE, Norwood VR 1989. Free-environment
rooms as alternative housing for squirrel monkeys. In Housing,
Care and Psychological Well-being of Captive and Laboratory Primates
Segal EF (ed), 102-114. Noyes Publications, Park Ridge
"Individual and gang cages were removed from two conventional
colony rooms and the monkeys [11 females and 5 males] were simply
released into the rooms. Immediately following the establishment
of these two free-environment rooms, a few monkeys incurred sprains
and broken teeth, probably resulting from falls. ... Two deaths
resulted from attacks by other monkeys."
Mendoza SP 1991. Sociophysiology of
well-being in nonhuman primates. Laboratory Animal Science
41, 344-349
The formation of same-sex groups of squirrel monkeys is rarely
accompanied by injurious aggression. Once unisexual groups have
stabilized, formation of larger heterosexual groups generally
proceeds smoothly.
Vermeer J 1997. The
formation of a captive squirrel monkey group. International
Zoo News 44, 146-149
"It is important that all females of a new [heterosexual]
group are related to each other, that is, that they come from
the same natal group. The introduction of unfamiliar females to
a small group with several females can result in much aggression
with severe injury." The minimum number of breeding females
in a group should be five to seven. A maximum of two adult males
should be added to these females. Groups of up to ten males can
be formed without many problems.
Williams LE, Abee CR 1988. Aggression
with mixed age-sex groups of Bolivian squirrel monkeys following
single animal introductions and new group formations. Zoo Biology
7, 139-145
"When introducing new animals to an established group,
the new animals should be unfamiliar with one another so as not
to form competing 'teams'. Additions to groups should include
enough animals so that aggression from the resident group will
be diffused, not concentrated on one or two animals." New
groups should be followed for a number of hours, even after an
initial decline in total agonistic interactions.
Vervet monkeys (Cercopithecus aethiops)
Else JG 1985. Captive propagation
of vervet monkeys (Cercopithecus aethiops) in harems. Laboratory
Animal Science 35, 373-375
Animals were placed randomly in ten single-male harem groups
with 5-10 females per enclosure. This "resulted in considerable
fighting among the females. Each group was gradually reduced over
a one year period to 2-4 females with their young. Three adult
females died during the [three year] study. All had been under
fairly continual harassment."
(2,2,a) Pair-housing: Practical Issues, Time Budget
Basile BM, Hampton RR, Chaudhry AM,
Murray EA 2007. Presence of a privacy divider increases proximity
in pair-housed rhesus monkeys. Animal Welfare 16(1), 37-39
"We observed twenty-five pairs of rhesus macaques (Macaca
mulatta) both with and without the presence of a privacy divider.
Monkeys spent significantly more time in the same half of the
pair-cage when the divider was in place. Subjects were fifty adult
rhesus macaque monkeys aged between 5 and 13 years, housed in
socially compatible pairs consisting of 18 male/male pairs, 2
female/female pairs, and 5 male/female pairs. We conclude that
the increase in proximity associated with the presence of the
privacy dividers reflects an increase in social tolerance and/or
attraction. A privacy divider may provide a safe haven and give
monkeys the ability to diffuse hostile situations before they
escalate."
Baker K, Bloomsmith M, Schoof V, Neu
K, Maloney M, Griffis C, Marinez M, Clay A 2005. Compairing pair-housing
options for caged rhesus macaques (Macaca mulatta). American
Journal of Primatology 66(Supplement), 180 (Abstract)
"Baseline behavioral data were collected on 20 singly-housed
adult rhesus macaques, 6 males and 14 females, all mother reared.
Isosexual pairs were then formed, and pairs were housed in three
form of pair caging balanced for order (6-8 weeks per phase):
FC (full contact: sharing adjacent cages), PC (protected contact:
access through perforated panels), and IC (intermittent contact:
full pairings separated several days/week)." While all forms
of pair housing increased affiliative behavior, levels were lower
in the protected contact than full contact or intermittent contact
housing condition. Levels of inactivity and anxiety-related behaviors
were higher in the protected than in the full contact or intermittent
contact condition, and full contact reduced anxiety-related behaviors
from baseline. Full contact and intermittent contact decreased
inactivity and increased aggression which occurred at higher level
in the intermittent than in the partial contact housing condition.
Abnormal behavior was affected only in females, with a decrease
from baseline only in the intermittent, and higher levels in the
partial than in the full contact condition. "Results suggest
that periodic separation may not detract from the benefits of
pair housing for rhesus macaques, but protected contact housing
may, balanced only by decreased aggression."
*Baumans V, Coke C,
Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt
V, Van Loo P 2007 Making Lives Easier for Animals in Research
Labs - Chapter
5.1. Pair Formation and Pair-Housing of Monkeys. Washington,
DC: Animal Welfare Institute
"The PI who does research with our pair-housed rhesus
insists that cage companions be separated during the night and
on weekends, so that they cannot fight and injure each other while
nobody is around. I would love to keep the animals together also
during the night, but cannot argue with the PI because I really
don't know if that would jeopardize the safety of the animals.
In our facility, compatible companions are allowed to remain together
also during the night, on weekends and holidays. This applies
for both female and male pairs, as well as for all animals who
have head cap implants. It has never happened that we found paired
animals injured or bruised when entering their room in the early
morning. I think there is no special risk when pairs spend the
night together without being supervised.
We also keep our male and female rhesus pairs together 24/7 and
encounter no problems related to aggression during the night.
At our facility, after pairs have been established, they are housed
together uninterruptedly. This includes male and female isosexual
pairs, and each species housed here, including rhesus, pigtails,
sooty mangabeys, squirrel monkeys, chimps, and cynos. We have
not noticed that paired companions fight during the night, on
weekends and holidays when nobody is around."
*Baumans V, Coke C,
Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt
V, Van Loo P 2007 Making Lives Easier for Animals in Research
Labs - Chapter
5.3.1. Post-Operative Care. Washington, DC: Animal Welfare
Institute
"It is my experience with rhesus macaques that it is advisable
to pair-house an animal after surgery as soon as possible with
his or her compatible companion. We do this especially with pairs,
after one of them had cranial implant surgery. It is the investigator's
and my own impression that the animals recover better from the
surgery stress when their familiar companion is with them than
when they are alone.
Close to 95 percent of our cyno population is pair-housed. The
animals are subjected to a lot of orthopedic procedures. There
have never been problems with the re-pairing of the animals after
surgery. We partition the pairs cage with a transparent panel,
which we remove after the treated companion has fully recovered
from anesthetic effects (usually 24 hours). It has never happened
that animals who had no surgery showed any negative behavioral
reactions toward their temporarily probably weaker cage mates."
*Baumans V, Coke C,
Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A, Reinhardt
V, Van Loo P 2007 Making Lives Easier for Animals in Research
Labs - Chapter
8.9. Pair-Housed Monkeys with Head Cap Implants. Washington,
DC: Animal Welfare Institute
"Our university tries to pair all rhesus macaques regardless
of cranial implants. Normally the pairs are established before
they have undergone surgery for head caps, but we have successfully
paired primates after surgery as well. Over a period of ten years,
we have had no incidents of damage to the implants. We have more
problems, with coils of head caps breaking, in single-housed than
in pair-housed rhesus. The head caps of pair-housed animals are
cleaner as they groom each other than those of individually caged
animals.
We have ten pair-housed male rhesus and long-tailed macaques with
head caps. The animals were 3 to 6 years old at the time of pair
formation. They are presently approximately 10 years old. Some
of them had head caps before they were paired, others got them
afterwards. It didn't seem to matter. In my experience, pair-housing
does not create a risk factor when the animals have head cap implants.
In all the time I've been working with these monkeys, they've
never damaged one another's head caps."
Brent L 1992. The effects of cage
size and pair housing on the behavior of captive chimpanzees.
American Journal of Primatology 27, 20
Paired subjects spent approximately 11% of the observation
time in socially directed behaviors.
Coe CL, Rosenblum LA 1984 Male dominance
in the bonnet macaque. In Social Cohesion. Essays Toward a
Sociophysiological Perspective Barchas PR, Mendoza SP (eds),
31-64. Greenwood Press, Westport
"During the first week [after formation of 5 male/male
pairs], the males spent a mean 29 percent of the observation time
within arm's reach, engaging in mutual grooming or passive body
contact."
Coe CL, Franklin D, Smith ER, Levine
S 1982. Hormonal responses accompanying fear and agitation in
the squirrel monkey. Physiology and Behavior 29, 1051-1057
Dominant and subordinate partners of male pairs did not differ
in their plasma cortisol levels.
Crockett CM 1998. Psychological well-being
of captive nonhuman primates. In Second Nature - Environmental
Enrichment for Captive Animals Shepherdson DH, Mellen JD,
Hutchins M (eds), 129-152. Smithsonian Institution Press, Washington
"Adult female long-tailed macaques benefit from social
enrichment through pairing with other females. Adult males also
have social needs, although they are more likely to express them
toward females. Many males ignore or behave aggressively toward
other males, although some male pairs are highly compatible. Housing
longtailed macaque males in paired caging with widely spaced grooming-contact
bars prevents aggressive pursuits and increases the success rate
of male pairing."
Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore
SA, Shiigi SM 1994. Psychological well-being in paired adult female
rhesus (Macaca mulatta). American Journal of Primatology
33, 89-99
Paired females spend in close proximity approximately 80% of
the time during the night, and 40% of the time during the day.
They engage in social interactions approximately 17% of the time.
Agonistic behaviors are very infrequent. "Health measures,
body weight gains, reproduction and immune responses do not differ
between dominant, subordinate, and single-housed females. Paired
females spend less time engaged in abnormal behavior than single-housed
females."
Gonzalez CA, Coe CL, Levine S 1982.
Cortisol responses under different housing conditions in female
squirrel monkeys. Psychoneuroendocrinology 7, 209-216
Dominant and subordinate partners of female pairs did not differ
in their plasma cortisol levels.
Gwinn LA 1996. A method for using
a pole housing apparatus to establish compatible pairs among squirrel
monkeys. Contemporary Topics in Laboratory Animal Science
35(4), 61
"Pair housing the animals has not interfered with research.
During nine treatments with an identical test compound, singly
housed animals lost significantly more weight on average than
did pair housed animals."
Hotchkiss CE, Paule MG 2003. Effect
of pair housing on operant behavior task performance by rhesus
monkeys. Contemporary Topics in Laboratory Animal Science
42(4), 38-40
"In conclusion, pair-housing monkeys is feasible for studies
involving operant behavior testing as a model for a variety of
complex brain functions. However, housing condition may affect
some test parameters, and this effect must be taken into consideration
during experimental design."
Jackson MJ 2001. Environmental enrichment
and husbandry of the MPTP-treated common marmoset. Animal Technology
(21-28)
"One disadvantage of isosexual pairing that we have encountered
is that temporary separation of the pair (e.g. for behavioural
monitoring) can precipitate fighting on re-introduction. If this
occurs we have found that a gradual re-association process, utilising
adjacent cages to permit visual and audio contact, and supervised
free running together, facilitates re-pairing."
McDonald KM, Ratajeski MA 2005. Pair-housing
of monkeys on behavioral studies. AALAS [American Association
for Laboratory Animal Science] 56th National Meeting Official
Program , 133 (Abstract)
"After periods of separation, we did not observe the animals
to act aggressively towards one other when re-paired, and injury
to head holder implants was never observed."
Murray L, Hartner M, Clark LP 2002.
Enhancing postsurgical recovery of pair-housed nonhuman primates
(M. fascicularis). Contemporary Topics in Laboratory
Animal Science 41(4), 112-113
"In many facilities, postsurgical protocol in the nonhuman
primate requires individual housing for a period of 2-10 days.
... Our goal was to allow [15 adult females] same-day return of
the postoperative [placement of vascular access port] candidate
to its paired environment. ... Change in hierarchy status, self-traumatic
events, weight loss or diarrhea did not occur in any of these
animals, and the incision sites healed unremarkably. The animals
ate and drank normally, and received their postoperative treatments
without problem (readily accepted oral medication). .. We conclude
that this practice of quick return to group status postoperatively
can be successfully employed, and it is a "best practice"
when working with these laboratory animals."
Majolo B, Buchanan-Smith H 2001. Psychological
wellbeing of common marmoset (Callithrix jacchus) females
living in same-sex pairs.
Primate Eye 74, 9-10
The behaviour of female pairs of common marmosets resembles
that of females living in family groups suggesting that this method
of housing does not compromise their welfare."
Reinhardt V, Cowley D, Eisele S, Vertein
R, Houser WD 1988. Pairing
compatible female rhesus monkeys for the purpose of cage enrichment
has no negative impact on body weight. Laboratory Primate
Newsletter 27(1), 13-15
"Keeping singly housed adult female rhesus monkeys in
compatible pairs for the purpose of cage enrichment does not affect
the animals' general health status as reflected in body weight."
Reinhardt V, Dodsworth R 1989. Facilitated Socialization
of Previously Single Caged Adult Rhesus Macaques (videotape with
accompanying text). Wisconsin Regional Primate Research Center,
Madison
Thirty scenes depict different adult rhesus monkeys [and one
adult, male stump-tailed macaque], each paired with a compatible
companion for up to two years. The following pair combinations
and research situations are shown: adult male/male, adult female/female,
adult male/juvenile male, adult female/juvenile female; experiments
requiring headcap implants, tethering, or in-home cage blood collection.
Presenting for in-homecage injection. Paired companions interact
with each other in various species-typical ways (e.g., grooming,
huddling, mounting, playing, yielding, sharing food) and make
use of perches and gnawing sticks. "Representing an every-changing,
yet predictable stimulus, a compatible companion does not lose
its boredom-reducing value over time."
Reinhardt V, Houser WD, Eisele S 1989.
Pairing previously singly caged rhesus monkeys does not interfere
with common research protocols. Laboratory Animal Science
39, 73-74
"Our experiences indicate that facilitated socialization
of previously singly caged rhesus monkeys offers an inexpensive
method of environmental enrichment that is practicable under common
management situations and numerous research conditions."
Reinhardt V 1990. Time budget of caged
rhesus monkeys exposed to a companion, a PVC perch and a piece
of wood for an extended time. American Journal of Primatology
20, 51-56
After 1.5 years paired partners spent an average of 23.5% of
the time interacting with the companion. Females were socially
more active than males.
Reinhardt V, Cowley D, Scheffler J,
Vertein R 1990. Living
continuously with a compatible companion is not a distressing
experience for rhesus monkeys. Laboratory Primate Newsletter
29(2), 16-17
Paired females had serum cortisol concentrations that did not
differ from single-housed females. "Dominant animals had
cortisol concentrations that did not differ from those of their
subordinate companions, indicating that neither dominant nor subordinate
partners experienced social distress."
Reinhardt V 1991. Social
enrichment for aged rhesus monkeys that have lived singly for
many years. Animal Technology 43, 173-177
"There is widespread concern that aged rhesus monkeys
who have been housed singly for a long time would do better living
alone than sharing a cage with a companion. Ten female and five
male rhesus monkeys, 22 to 33 years old and deprived of physical
contact with any other conspecific for more than 10 years, were
socialized with weaned infants or with each other using two standard
methods of pairing. Pairs were compatible in every case throughout
a one year follow-up period."
Reinhardt V, Pape R, Zweifel D 1991.
Multifunctional cage for macaques housed in pairs or in small
groups. American Ass for Lab Animal Science Bulletin [Contemp
Topics in Laboratory Animal Science] 30(5), 14-15
Double-cage units were modified to provide optimal housing
conditions for pair-housed macaques. Perch installation allows
normal operation of the squeeze-back; a privacy panel offers optional
visual seclusion.
Reinhardt V, Reinhardt A 1991. Impact
of a privacy panel on the behavior of caged female rhesus monkeys
living in pairs. Journal of Experimental Animal Science
34, 55-58
"Paired partners spent significantly more time in close
proximity when the privacy panel was provided. At the same time,
they were more engaged in affiliative interactions while the incidence
of agonistic interactions tended to decrease."
Reinhardt V, Hurwitz S 1993. Evaluation
of social enrichment for aged rhesus macaques. Animal Technology
44, 53-57
The 31-36 years old "subjects preferred to stay in close
proximity with their companion even though this reduced their
available cage space. They spent on average 21% of the time interacting
with the companion. Sharing a cage with a compatible conspecific
did not jeopardize the subjects' general health, as reflected
in their body weight development."
Reinhardt V 1994. Social
enrichment for previously single-caged stumptail macaques.
Animal Technology 5, 37-41
Female pairs and male pairs engaged in non-injurious species-typical
activities 25% and 17% of the time.
Reinhardt V 1994. Continuous pair-housing of caged Macaca
mulatta: Risk evaluation.
Laboratory Primate Newsletter 33(1), 1-4
"Pairs were compatible in 88% of cases during the follow-up
period of 1 to 6.3 years. There were no indications that long-term
compatibility of male pairs was less than that of female pairs."
Reinhardt V 1994. Pair-housing
rather than single-housing for laboratory rhesus macaques.
Journal of Medical Primatology 23, 426-431
First-year compatibility was 88% in adult female-female pairs,
80% in adult male-male pairs. Adult-infant pairs were compatible
in 92% of 15 male-infant pairs, and in 94% in 65 female-infant
pairs. The incidence of serious injury was 0.7% (2/272) during
the first year after pair formation.
Reinhardt V 1996. Frequently
asked questions about safe pair-housing of macaques. Animal
Welfare Information Center (AWIC) Newsletter 7(1), 11
Nine frequently asked questions regarding safe pair-housing
protocols for macaques are addressed.
Reinhardt V, Reinhardt V 2000. Meeting
the "social space" requirements of pair-housed primates.
Laboratory Primate Newsletter 39(1), 7
"Social space is the space required by a subordinate partner
to buffer potential social tension, by increasing the distance
to a dominant counterpart. At a minimum, pair-housed animals should
be allocated at least twice the cage space that is legally required
for single-housing."
Reinhardt V 2002. Addressing
the social needs of macaques used for research. Laboratory
Primate Newsletter 41(3), 7-10
"The present paper summarizes the author's experiences
transferring a colony of rhesus macaques (Macaca mulatta) from
individual- to pair-caging. ... The implementation of pair-housing
as standard caging at Wisconsin RPRC was not excessively expensive
in terms of work time and material. It was not a hindrance to
active research; rather it improved the animals' behavioral health
and made them more species-representative research models . A
total of 726 pairs were formed involving 817 different animals,
yet no indication was found that this rendered research data collected
from them useless due to confounding variables such as stress
or disease."
Roberts SJ, Platt ML 2005. Effects
of isosexual pair-housing on biomedical implants and study participation
in male macaques. Contemporary Topics in Laboratory Animal
Science 44(5), 13-18
"Social housing has been shown to contribute to the psychological
well-being and physical health of captive primates, and this factor
has led to United States Department of Agriculture guidelines
requiring facilities to address the social needs of primate species
known to live socially in nature as long as doing so does not
endanger the animals or interfere with research goals. Although
pair-housing is the best way to provide social enrichment, many
researchers and facilities are hesitant to implement it, particularly
in biomedical research contexts where implanted devices or behavioral
performance might be compromised. In order to study the effects
of pair-housing on biomedical implants and study participation,
we collected data from a group of isosexually pair-housed male
macaques (adult and subadult) with 1) cranial and eye implants
and 2) controlled access to water as means of motivating subjects
to participate in psychophysical studies. Implants, study participation,
and weight gain were not adversely affected by pair-housing. Our
results support the use of pair-housing as social enrichment for
macaques with biomedical implants and controlled access to water."
Consistent directional dominance behavior served to assess potential
partner compatibility. Of 15 rhesus diads, 12 [80%] were compatible.
One cyno diad was also tested and was compatible. Compatibility
was ascertained over a period of 0.8 - 3.3 years." One monkey,
however, occasionally exhibited noninjurious self-biting when
someone other than his usual handler took him out of his cage,
and two other monkeys occasionally placed in their cages when
agitated."
Schapiro SJ, Bloomsmith MA, Kessel
AL, Shively CA 1993. Effects of enrichment and housing on cortisol
response in juvenile rhesus monkeys. Applied Animal Behaviour
Science 37, 251-263
"Social housing condition [single vs. pair] also did not
affect cortisol."
Schapiro SJ, Bloomsmith MA, Porter
LM, Suarez SA 1996. Enrichment effects on rhesus monkeys successively
housed singly, in pairs, and in groups. Applied Animal Behaviour
Science 48, 158-172
"Subjects were more socially oriented when pair-housed
than when living in small groups. Subjects used enrichment less
frequently when housed in groups. The data suggest that the presence
of a social partner(s) led to more beneficial changes in behavior
than did the provision of inanimate enhancements."
Sheehan J, Ziegelhofer T, Henn S,
Miyamoto M, Vanterpool I 2005. A novel caging method for collecting
telemetry data from pair-housed monkeys. AALAS [American Association
for Laboratory Animal Science] 56th National Meeting Official
Program , 117 (Abstract)
Caging method is described that allows telemetric measurements
[ECG and blood pressure] of long-tailed macaques housed in pairs.
"The first method consisted of modifying the current cages
to add a wire mesh tunnel constructed above the two adjacent cages,
with sliding doors on either end so the monkeys could be intermittently
paired. The second method for improvement with these modified
cages was to compare results if we permanently placed a telemetered
and a non-telemetered pair of monkeys in the cages and collected
data using the distributed receiver array which allows for two
receivers to be configured to one animal." No differences
were noted in the data collected nore were any artifacts created
by application of the second uninterrupted pair-housing method.
Shively CA 2001. Psychological
well-being of laboratory primates at Oregon Regional Primate Research
Center. Web sit link in Willamette Week (Portland),
March 21, 2001
"I was exposed to no protocols that required social isolation
during my visit to the ORPRC. Rather, investigators were not giving
priority to the social needs of the monkeys. For example, monkeys
in virus studies at other institutions are housed socially with
animals with similar virus load. Animals on timed mating protocol
do not need to be housed alone. Animals in protocols requiring
food restriction can be pair housed and separated from cagemates
for 8 hrs during the day when food is accessible. They can be
socially housed the other 16 hrs/day. ... The IACUC should use
its authority to decline approval of protocols that do not demonstrate
a detailed defense of single caging."
Yanagihara Y, Matsubayashi K, Matsuzawa
T 1994. Environmental enrichment in Japanese monkeys: Feeding
device [Japanese text with English summary]. Primate Research
10, 95-104
"The two monkeys spent the night in same living unit,
while they spontaneously separated from each other in the different
units during feeding time.
(2,2,b) Pair-housing: Pair formation
Baboons (Papio spp.)
Bourgeois SR, Brent L 2005. Modifying
the behaviour of singly caged baboons: evaluating the effectiveness
of four enrichment techniques. Animal Welfare 14, 71-81
Seven singly caged adolescent [mean age: 4.2 years] male baboons
were studied. Pairs were formed by introducing sedated partners
in the same cage. "Pairing was successful for all seven individuals,
with no serious injuries or overt aggression observed."
Jerome CP, Szostak L 1987. Environmental
enrichment for adult, female baboons (Papio anubis). Laboratory
Animal Science 37, 508-509
"Each baboon was placed in a cage with another baboon
for 3-4 hours, two or three times per week. The same pairs consistently
visited each other in either animal's cage. No significant aggression
occurred."
Gorillas (Gorilla spp.)
Gould JE 1990. Conspecific introduction,
socialization, and attempts to breed a solitary-raised, silverback
male gorilla. Proceedings of the Columbus Zoo Gorilla Workshop,
56-79
"Even though the silverback Colossus had not had an opportunity
to interact with any other gorilla since infancy, his introduction
to the adult female conspecific Muke was very successful."
The careful pair formation procedure is described.
Macaques (Macaca spp.)
Abney DM, Weed JL 2006. Methods for
successfully pair housing adult male rhesus macaques (Macaca
mulatta). American Journal of Primatology 68(Supplement
), 59 (Abstract)
The successful same-sex pairing of 34 male rhesus macaques
is described. "Animals were socialized in different age combinations,
consisting of adult/adult, adult/sub-adult, and adult/juvenile.
.. The pairs started with a clear panel, allowing the animals
to see one another, but not touch. Next, they were given a mesh
panel, which allowed finger touch access. Grooming bars were the
final panel used before the pair was given full, un-restricted
access. Pairs were deemed successful if no serious fighting or
injury occurred within one weeks time. Out of 56 rhesus socializations
attempted which included at least one adult, 34 were successful
(61%)."
Anonymous 2006. Pair
formation and reintroduction of temprarily separated partners
A discussion on the Laboratory Animal Refinement & Enrichment
Forum. Laboratory Primate Newsletter 1, 11-12
"To sum up, it seems advisable to monitor the reintroduction
of temporarily separated partners very carefully, and if possible,
to allow the animals to first recognize each other before they
are reunited as a pair. There is no good reason to believe that
male cynos are less suitable for isosexual pair-housing than rhesus.
If and how experimentally-induced pathophysiological processes
affect the compatibility of pairs needs to be explored."
Byrum R, St. Claire M 1998. Pairing female Macaca nemestrina. Laboratory Primate Newsletter 37(4),
1
Twenty-four adult pig-tailed macaques were successfully transferred
from single- to pair-housing arrangements following the establishment
of rank relationships during a semi-contact familiarization period.
"We have observed no serious fighting and wounding in our
pairs, neither at the moment of introduction nor during follow-up
observations of up to two years."
Coe CL, Rosenblum LA 1984 Male dominance
in the bonnet macaque. In Social Cohesion. Essays Toward a
Sociophysiological Perspective Barchas PR, Mendoza SP (eds),
31-64. Greenwood Press, Westport
"As usually occurs when unfamiliar males first meet, agonisitc
behaviors related to the establishment of dominance relations
occurred at pair formation. The aggressive incidents were limited,
usually involving threats and pursuit behavior. .. More typically,
one animal submitted and indicated his subordinate status through
communicative gestures. In the first week following pair formation,
the occurrence of aggressive behavior subsided almost entirely."
Crockett CM, Bowers CL, Bowden DM,
Sackett GP 1994. Sex differences in compatibility of pair-housed
adult longtailed macaques. American Journal of Primatology
32, 73-94
Prefamiliarized partners were paired without ascertaining that
they had established their dominance-subordination relationship.
Newly formed pairs were separated for 17 hours and subsequently
reintroduced daily during a study period of 23 days. Under these
circumstances, no female pair but seven [47% of 15] male pairs
were separated because of fighting and wounding.
Crockett CM, Lee GH, Thom JP, Bentson
KL 2005. Does temperament similarity predict compatibility of
same-sex and opposite-sex rhesus macaques paired in grooming/contact?
American Journal of Primatology 66(Supplement), 58 (Abstract)
Partner compatibility was not significantly associated with
temperament.
*Doyle LA, Baker
KC, Cox LD 2008. Physiological and behavioral effects of social
introduction on adult male rhesus macaques. American Journal
of Primatology 70, 1-9
Potential partners of four adult rhesus macaque pairs were
first familiarized in cages in which partners were separated by
a panel consisting of bars spaced 2 cm apart. The eight males
were all implanted with biotelemetry devices for remote heart
rate monitoring. After 24 hours, as neither persistent aggression
nor wounding was observed, each pre-familiarized pair was introduced
into full contact by removing the barred panel. All four introductions
were successful and subjects showed no physiological (fecal cortisol
concentration and heart rate) or behavioral signs (pathological
behavior) of stress, or psychological indices of distress (depressive/anxiety-related
behavior) not only during the introduction process but also over
a follow-up period of 18 months. No overt aggression was displayed
at all during the first two hours following pair formation. Aggressive
interactions were minimal thereafter. Only one bite laceration
was incurred 14 weeks after pair formation. The partners of this
pair were maintained in the home cage with the barred panel to
allow wound healing; they were subsequently placed again into
full contact with no further complications. "The results
of this study may be of practical use for designing and monitoring
social introductions and suggest that managers should not dismiss
the feasibility of successful pairing of adult male rhesus macaques."
Eaton GG, Kelley ST, Axthelm MK, Iliff-Sizemore
SA, Shiigi SM 1994. Psychological well-being in paired adult female
rhesus (Macaca mulatta). American Journal of Primatology
33, 89-99
Partners were paired after a noncontact familiarization period.
Pairs were compatible in 86% of 21 cases.
Line SW, Morgan KN, Markowitz H, Roberts
J, Riddell M 1990. Behavioral responses of female long-tailed
macaques (Macaca fascicularis) to pair formation. Laboratory Primate Newsletter 29(4),
1-5
Potential partners were familiarized in a noncontact situation
prior to pairing. Five of six pairs tested were compatible during
a five to six months study period.
McLean M, Morris J, Watson E, Gavetti
D, Marshall S 2006. Retrospective evaluation of pair-housing juvenile
and adult cynomolgus macaques in a pharmaceutical environment.
AALAS [American Association for Laboratory Animal Science]
57th National Meeting Official Program , 148 (Abstract)
"Our experience and data suggest that pair formation in
juvenile and adult cynomolgus male and female macaques has been
successful and as allowed us to provide social housing in a pharmaceutical
environment."
McMillan J, Maier A, Tully L, Coleman
K 2003. The effects of temperament on pairing success in female
rhesus macaques. American Journal of Primatology 60(Supplement),
95
http://www.asp.org/asp2003/abstractDisplay.cfm?abstractID=576&confEventID=554
“We assessed temperament in these monkeys, along with their
two partners, by measuring their reaction to novel objects (e.g.,
a brightly colored novel toy) presented to them in their home
cages. Every monkey received a score from 0-6 based on her reaction
to the novelty. .. Temperament scores were more similar between
the focal monkeys and their successful partner than their unsuccessful
partner. These results suggest that assessing temperament with
a simple testing paradigm may be useful in forming successful
pairs.“
Niemeyer C, Eaton, GG, Kelley ST1998.
Practical aspects of the program to promote psychological well-being
in nonhuman primates at the Oregon RPRC. In Proceedings of
the Third International Conference on Environmental Enrichment
Hare VJ, Worley E (eds), 345-354. The Shape of Enrichment
"New pairs are formed by moving both [pre-familiarized]
individuals to a new location because monkeys housed in individual
cages appear to become territorial about their cages."
Reaves ME, Cohen J 2005. Primate pairing
under less than ideal circumstances. Tech Talk 10(5), 1-2
"Of the six male cynomolgus monkeys in our group, we were
able to create three stable pairs. The animals share food, and
although we have had some minor bumps and bruises, there have
been no serious injuries. We later reproduced these results with
our vervet colony and after the quarantine process with all new
arrivals.".
Reinhardt V, Houser WD, Eisele S,
Champoux M 1987. Social
enrichment with infants of the environment for singly caged adult
rhesus monkeys. Zoo Biology 6, 365-371
"Twenty-nine weaned rhesus monkey infants were removed
from breeding troops to avoid overcrowding and were placed with
unfamiliar singly caged adults" without prior familiarization.
"Adult-infant pairs were compatible in 90% of cases. Compatibility
depended neither on the sex, age, and origin of the adult nor
on the sex of the infant."
Reinhardt V 1989. Behavioral responses
of unrelated adult male rhesus monkeys familiarized and paired
for the purpose of environmental enrichment. American Journal
of Primatology 17, 243-248
"Potential companions were first given the opportunity
to establish clear-cut rank relationships during a 5-day period
of noncontact familiarization. Only then were they paired in a
different double cage. Rank relationships were confirmed within
the first 6 minutes after pairing without the occurrence of any
biting and fighting. It stands to reason that the risk of injury,
intrinsically associated with pairing, can be minimized if only
those dyads are selected whose partners show unequivocal signs
of an established rank relationship during a period of noncontact
familiarization."
Reinhardt V 1991. Agonistic behavior responses of socially experienced,
unfamiliar adult male rhesus monkeys (Macaca mulatta) to
pairing. Laboratory Primate
Newsletter 30(1), 5-7
"The present data demonstrate that unfamiliar adult male
rhesus monkeys may generally be paired directly with each other
without undue risk provided partners have previously lived with
another male companion. This is congruent with the findings made
with adult females."
Reinhardt V 1994. Social
enrichment for previously single-caged stumptail macaques.
Animal Technology 5, 37-41
10 females and 6 males were isosexually introduced following
the establishment of rank relationships during a three-day non-contact
familiarization period. "Pair formations did not entail serious
antagonism; instead companions engaged in conciliatory interactions."
Watson LM 2002. A successful program for same- and cross-age
pair-housing adult and subadult male Macaca fascicularis. Laboratory Primate Newsletter 41(2),
6-9
Isosexual pairs of adult males, adult male/juvenile male and
adult females were established and pair compatibility ascertained
throughout follow-up periods of 1 month to 3 years. Partners were
introduced after a carefully supervised noncontact familiarization
period in a specific pair formation cage placed in an location
other than the animals' homeroom. Of 31 adult male pairs tested,
29 [94%] were compatible; two pairs had to be separated because
"one animal in each pair sustained injuries during minor
fighting."
Marmosets (Callithrix spp.)
Majolo B, Buchanan-Smith HM, Morris
K 2001. Factors affecting the successful pairing of
unfamiliar common marmoset (Callithrix jacchus) females. Primate Eye 73, 12-13
"Data on the formation of 46 common marmoset (Callithrix
jacchus) female pairs in a laboratory were analysed. The success
rate was 83%. The age of the females appears to be a critical
factor in success rate, and aggression is lower if one member
of the pair is not yet sexually mature (i.e. < 12 months).
The results of this study show that pairing unfamiliar common
marmoset females can be accomplished safely to avoid single housing
when natural social grouping is not feasible."
Squirrel monkeys (Saimiri spp.)
Gwinn LA 1996. A method for using
a pole housing apparatus to establish compatible pairs among squirrel
monkeys. Contemporary Topics in Laboratory Animal Science
35(4), 61
Successful pair formation protocol in a pole-and-collar housing
system is described.
Vervet monkeys (Cercopithecus spp.)
Dansie C, Galvao AV, McKain J, Despain
KE 2004. African Green nonhuman primate enrichment. American
Association for Laboratory Animal Science 55th National Meeting
Official Program, 129
“Selected pairs are housed with plexi-panels between them
for at least one week. At the end of this adaptive periods, pairs
are allowed access to each other by removal of the grated panels
separating them for a supervised period of one hour. The daily
amount of time monkeys access each other is increased gradually
until transition to pair-housing is complete.”
Gerald MS, Weiss A, Ayala JE 2006.
Artificial colour treatment mediates aggression among unfamiliar
vervet monkeys (Cercopithecus aethiops): a model for introducing
primates with colourful sexual skin. Animal Welfare 15(4),
363-369
"Painting the scrotum dark led to more aggression when
these males were paired with dark coloured males and less aggression
when these males were paired with pale coloured males. These findings
suggest a practical and inexpensive means of reducing the likelihood
of aggression when introducing new animals."
(2,3)
Grooming-Contact Caging
Crockett CM, Bellanca RU, Bowers CL,
Bowden DM 1997. Grooming-contact bars provide social contact for
individually caged laboratory macaques. Contemporary Topics
in Laboratory Animal Science , 53-60
Pair formation of adult long-tailed macaques was accomplished
by using widely spaced, vertical grooming-contact bars that allow
physical contact [but no copulation] but prevent pursuit by one
animal into the other's cage. Pair compatibility was 100% in all
cases except unfamiliar male pairs (86%).
(2,4) Positive Interaction with Humans
Abney D, Conlee K, Cunneen M, Down
N, Lang T, Patterson-Kane E, Skoumbourdis E, Reinhardt V 2006.
Human-animal
relationship in the research lab: a discussion by the Refinement
and Enrichment Forum. Animal Technology and Welfare
5(2), 95-98
"I think an affectionate human-animal relationship
makes a huge difference for the animals because it helps them
overcome anxiety and fear in disturbing or distressing situations."
"The stress resulting from a neutral or negative relationship
between investigator/technician and animal is bound to affect
the research data collected from the animal subject, but the research
industry is not yet taking this methodological flaw seriously."
Anonymous 2006. Primate passion An
interview with Karen MacLeod, RVT, AALAS Northern California Branch
Technologist of the Year 2006. Lab Animal 35(9), 6
When asked how she deals with attatchment to animals in her
care: "Its hard because I am passionate about what I do and
because our animals are long-term. It is important to be attached
and there are certainly days when I am in tears, but I think if
I ever felt unaffected by euthanizing our animals, it would be
time for me to leave. As hard as it is to be passionate about
what I do, I think it is a serious job requirement."
Anonymous 2003. Personnel
/ Animal Relationships: Affectionate or Neutral: A Discussion.
Laboratory Primate Newsletter 42(1), 14-15
"Having a close relationship with your animals is necessary
to regard them as living beings, rather than biological test tubes.
As such, you are more careful and patient, and will think more
about what the procedures mean to the animals. You will get more
creative in finding animal friendly alternatives for the procedures
you need to do on the animals. You will thus increase the well-being
of your animals and, by doing so, make better research subjects
and increase the validity of the test results. .. There was a
consensus that the emotional attachment provides an assurance
that the animals receive optimal care, both physically and behaviorally.
.. Concern was expressed that establishing an affectionate relationship
with experimental subjects and knowing them as individuals would
hamper ones impartiality and capacity to be objective when observing
and registering their behavior. A caregiver strongly objected:
It seems to me that we get hung up on trying to divorce our emotions
from what we hope to be our objectivity. I do not think that any
normally functioning human being in the world does anything for
any reason other than emotional. Sure, research is done to answer
questions, but isn't the premise of all research to make human
(or animal) lives better? If you want to make lives better, it's
because of emotion, not because you are logically attached to
life."
Baker KC 1997. Human interaction as
enrichment for captive chimpanzees: A preliminary report. American
Journal of Primatology 42, 92
Simple, unstructured affiliation between humans and chimpanzees
has a powerful impact on well-being, promoting activity and relaxed
conspecific interactions and ameliorating behavioral disorders.
*Baumans V, Coke
C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,
Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals
in Research Labs - Chapter
2.3.1. Affection for Animals. Washington, DC: Animal Welfare
Institute
"Animal care personnel and researchers should be encouraged
to develop affectionate relationships with their animals. Having
such a relationship assures that you regard the animals as living
beings, rather than biological test tubes. As such, you will be
more careful and more patient. You will think more about what
the experimental procedure implies to the animals. You will get
more creative in refining procedures that are normally stressful
or distressing to the animals. You will thus enhance their well-being
and, by doing so, you will increase the scientific validity of
the research results.
If you are not kind to your animals, make no attempt to enrich
their boring, often depressing living quarters by addressing species-typical
behavioral and social needs, and never show any kind of affection
towards them (for example by offering them food treats from time
to time), then I really don't think that you should work in an
animal research laboratory."
*Baumans V,
Coke C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt
A, Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals
in Research Labs - Chapter
2.3.2. Giving Animals Names. Washington, DC: Animal Welfare
Institute
"Naming the animals helps me realize that I am working
with sentient beings who deserve my consideration of their well-being.
I guess, we can all relate much better to names than to numbers,
and we tend to treat named versus numbered animals accordingly.
The naming of animals in research labs could serve as a safeguard
for optimal animal care.
We have an investigator who is against the naming of rabbits assigned
to her research protocol. The PI is afraid that, when bonding
with her research subjects, we add a variable that is detrimental
to performing research. Our staff feels that this is an antiquated
mentality and we are all standing strong in our position of naming
all animals in our charge!"
Bayne K 2002. Development
of the human-research animal bond and its impact on animal well-being.
ILAR [Institute for Laboratory Animal Research] Journal
43(1), 4-9
The various roots of human-animal bonding in the research laboratory
setting are reviewed. "The development of these relationships
is enriching to both personnel and animals inasmuch as people
who care about their animals are committed to promoting and ensuring
the well-being of those animals."
Bayne K, Dexter SL, Strange GM 1993.
The effects of food treat provisioning and human interaction on
the behavioral well-being of rhesus monkeys (Macaca mulatta).
Contemp Topics in Laborat Anim Sci 32(2), 6-9
"The effects of human interaction and food supplementation
appear to be protracted, resulting in a reduction of pathology
[behavioral disorders] even after the enrichment is removed."
Bennett BT 1990. Alternative
methodologies. In Essentials for Animal Research: A Primer
for Research Personnel Bennett BT, Brown MJ, Schofield JC
(eds), 13-25. USDA, National Agricultural Library, Beltsville
"Almost every animal commonly used in the laboratory responds
positively to a little tender loving care. It's inexpensive, readily
portable, safe even at the highest doses and spreads rapidly through
the staff."
Boccia ML, Broussard C, Scanlan J,
Laudenslager ML 1992 Practice makes predictable. In The Inevitable
Bond: Examining Scientist-Animal Interactions Davis H, Balfour
AD (eds), 153-170. Cambridge University Press, Cambridge
"In our laboratory, we have made it a point to minimize
the human-animal interactions, assuming that by minimizing interactions,
we optimize experimental conditions by eliminating confounding
handling effects. The results presented here, however, suggest
that it may be necessary to reverse this thinking."
Choi GC 1993. Humans enrich the lives
of lab baboons. WARDS Newsletter Summer, 3-7 & 13
"The reduction in cage painting and banging was dramatic
and remarkable" after the single-housed animals received
more attention from the attending personnel.
European Economic Community 1986.
Council
Directive 86/609, Annex II Guidelines for Accommodation and Care
of Animals. Official Journal of the European Communities
L358 , 7-28
"The performance of an animal during an experiment depends
very much on its confidence in man, something which has to be
developed. It is therefore recommended that frequent contact should
be maintained so that the animals become familiar with human presence
and activity."
Home Office 1989. Animals
(Scientific Procedures) Act 1986. Code of Practice for the Housing
and Care of Animals Used in Scientific Procedures. Her
Majesty's Stationery Office, London
"Where appropriate, time should be set aside for handling
and grooming. All staff, both scientific and technical, should
be sympathetic, gentle and firm when dealing with the animals."
Jensvold ML 2007. Promoting positive
interactions between chimpanzees (Pan troglodytes) and
caregivers. Laboratory Primate Newsletter 46(1), 1-4
"We tested our contention that when caregivers use chimpanzee
behavior, more positive interactions result.
Mahoney CJ 1992. Some thoughts on
psychological enrichment. Lab Animal 21(5), 27,29,32-37
"A spark of compassion in any one person towards the animals
can be fanned into flames of empathy with the right encouragement,
without destroying the primary research goals. In my experience
[as attending veterinarian] it is utterly impossible, however,
to make an uncaring person caring. Such people are not suited
for this line of work (p. 35). .. There should be no sharp demarcation
between 'good guys' and 'bad guys.' All employees, to some extent
must share the work. Nonhuman primates are quick to forget, or
perhaps forgive, the momentary fear or resentment they feel towards
a human being who has just subjected them to an unpleasant experience
if a strong bond of trust already exists with that person."
Morton DB, Jennings M, Buckwell A,
Ewbank R, Godfrey C, Holgate B, Inglis I, James R, Page C, Sharman
I, Verschoyle R, Westall L, Wilson AB 2001. Refining procedures
for the administration of substances. Laboratory Animals
35, 1-41
"Where substances are administered infrequently but on
a long-term basis handling the animals during routine daily husbandry
will help reduce stress when subsequently dosing them. In general,
staff should be encouraged to handle animals as much as possible."
National Research Council 1996. Guide for the
Care and Use of Laboratory Animals. National Academy Press,
Washington
"The animal technician's and caregiver's roles are pivotal
to the social support of primates, particularly animals that are
singly caged. ... When they must be housed alone, other forms
of enrichment should be provided to compensate for the absence
of other animals, such as safe and positive interaction with the
care staff."
Reinhardt V 2003. Compassion for animals
in the laboratory: Impairment or refinement of research methodology.
Journal of Applied Animal Welfare Science 6, 123-130
http://www.awionline.org/Lab_animals/biblio/jaaws10.html
“Compassion for animals used in research, testing and teaching
should not be regarded as subjective but as a sound methodological
base for scientifically valid animal research.”
Reese EP 1991. The role of husbandry
in promoting the welfare of laboratory animals. In Animals
in Biomedical Research Hendriksen CFM, Koeter HBWM (eds),
155-192. Elsevier, Amsterdam
"An important, and often neglected, source of social enrichment,
especially when animals must be isolated from conspecifics, is
attention from caretakers and technicians. That many scientists
lack detailed information about their animals, especially their
behavior, is distressing and reflects a serious disregard for
the single most important element of their research. The animal
is the key to the entire experiment. ... The proper handling of
laboratory animals is as essential to the collection of valid
data as it is to the animals' comfort and well-being. The more
the animal is handled properly, the more docile it becomes, especially
if handling begins at an early age. Conversely, the more an animal
is mishandled, the more difficult, frightened, and aggressive
it is likely to become ... Successful shaping requires the right
attitude, a thorough understanding of the individual animal and
of the task to be performed, and clinical skills. There is only
one 'right' attitude, and that is respect for the individual animal.
... My students must name their animals, and I do not let them
put an animal in the apparatus until they show me it will eat
from their hands."
Russow L-M 2002. Ethical
implications of the human-animal bond. ILAR [Institute
for Laboratory Animal Research] Journal 43(1), 33-37
"Researchers must continue to question the barriers that
have traditionally been errected against forming HABs in the name
of objectivity and to investigate seriously the ways in which
fostering the formation of HABs can promote animal welfare without
compromising the scientific respectability of research."
Sokol KA 1993. Commentary: Thinking
like a monkey - "primatomorphizing" an environmental
enrichment program. Lab Animal 22(5), 40-45
"We encouraged animal caretakers to visit the animals
at times other than their normal routines to reinforce positive
interactions and associations. Instead of identifying the monkeys
by just a tattoo number, we gave them names. Thus, we could refer
to them as individuals and better identify them for health considerations."
Southey ER, Baldwin CM 2006. Socialisation
of rhesus macaques at CFM. Animal Technology and Welfare
5(2), 119-122
The Centre for macaques in England is an example of best practice
in the care and welfare of old world primates in addition to an
evolving centre for the education and training of people working
in the area of primate research. Husbandry techniques and socialisation
of the macaques are described. Socialisation comprises of hand
feeding through cage room and lobby bars, going into the playpen
to hand out food and sitting in with the animals and interacting
on a closer basis.
Wolfle TL 1987. Control of stress
using non-drug approaches. Journal of the American Veterinary
Medical Association 191, 1219-1221
"Human interaction with monkeys and apes is essential
for the well-being of the animal, data validity, and ease of handling."
The 'social bond' with the animal "conveys to the animal
a quiet sense of assurance on which coping strategies can be developed
for dealing with other stressful aspects of the laboratory."
Wolfle TL 2002. Introduction.
ILAR [Institute for Laboratory Animal Research] Journal
43(1), 1-3
"I was encouraged not to assign names to the many rhesus
monkeys in my charge. I was admonished that the animals are research
subjects, not pets. The concern was that having names for the
animals might blur this distinction between a research subject
and a pet. .. It did not seem possible to remain distant - emotionally
isolated - from the animals. In fact, the inevitable closeness
that resulted from those intimate interactions was precisely what
made us capable of doing what we were asked to do. ... Eventually,
we all came to know that F49 was Sam, A12 was Rosie, and Z13 was
Curious. ... Such attachments are the results of compassionate
people doing their job right."
(3) Promoting Intelligent Behavior: Positive Reinforcement Training
Home Office 1989. Animals
(Scientific Procedures) Act 1986. Code of Practice for the Housing
and Care of Animals Used in Scientific Procedures. Her
Majesty's Stationery Office, London
"The least distressing method of handling is to train
the animal to co-operate in routine procedures. Advantage should
be taken of the animal's ability to learn."
Prentice ED, Zucker IH, Jameton A
1986. Ethics of animal welfare in research: The institution's
attempt to achieve appropriate social balance. The Physiologist
29, 1&19-21
"Physical restraint procedures should be used on awake
animals only after alternative procedures have been considered
and found to be inadequate. If a restraint will be utilized the
animal should be trained or conditioned to the restraining device,
using positive reinforcement, prior to the beginning of the experiment"
*Baumans V, Coke
C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,
Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals
in Research Labs - Chapter
7.2. Injection and Blood CollectionHow to minimize Stress Reactions.
Washington, DC: Animal Welfare Institute
"If the animals are under stress while you are working
with them, there is a great risk that they show aggressive reactions
to you, in an attempt to get away from the stressful situation.
One of the conditions of successful and safe positive reinforcement
training is a stress-free work environment, both for the animal
and for you. This means, neither the animal nor you should be
under the emotional influence of fear, apprehension or frustration.
These emotions are dangerous when your handle monkeys or, for
that matter, any other animals.
You should reach a stage when you know that you can trust
the trainee while you work with him or her. This does not mean
that you should not be alert, but any traces of mistrust and fear
puts you into a seriously dangerous position. Do not work with
an animal, unless you have trust in him or her! For your additional
safety, you will always have to make sure that your interaction
with the trainee will not be disturbed or disrupted by any unexpected
event, such as personnel entering the room or loud personnel passing
in hallways."
Chambers DR, Gibson TE, Bindman L,
Guillou PJ, Herbert WJ, Mayes PA, Poole TB, Wade AJ, Wood RKSBC
1992. Guidelines on the Handling and Training of Laboratory
Animals. Universities Federation for Animal Welfare, Potters
Bar
Very helpful outline of what has to be taken into consideration
when training animals to cooperate during handling procedures.
"Non-human primates, particularly the larger macaques, vervets,
baboons and apes, are readily trained to cooperate in procedures
such as presenting an arm for blood collection."
Home Office 1989. Animals
(Scientific Procedures) Act 1986. Code of Practice for the Housing
and Care of Animals Used in Scientific Procedures. Her
Majesty's Stationery Office, London
" The least distressing method of handling is to train
the animal to co-operate in routine procedures. Advantage should
be taken of the animal's ability to learn."
Klein HJ, Murray KA 1995. Part C.
Restraint. In Nonhuman Primates in Biomedical Research - Biology
and Management Bennett BT, Abee CR, Henrickson R (eds), 286-297.
Academic Press, New York
"The importance of training and adaptation cannot be overemphasized.
This not only reduces stress to the animal but promotes safety
and quality data collection."
Laule GE, Desmond T 1998. Positive
reinforcement training as an enrichment strategy. In Second
Nature - Environmental Enrichment for Captive Animals Shepherdson
DH, Mellen JD, Hutchins M (eds), 302-313. Smithsonian Institution
Press, Washington
Principles of positive reinforcement training are clearly outlined
and applications reviewed. "Animals are reinforced with pleasurable
rewards for the desired behavioural response. Operationally, this
means that positive alternatives are exhausted before any kind
of negative reinforcement is used." Punishment "is only
appropriate in a situation that is life threatening for person
or animal. ... Positive reinforcement training does not require
any food deprivation. ... This training regime relies on voluntary
cooperation by the animal to be successful."
Laule G 1999. Training laboratory
animals. In The UFAW [Universities Federation for Animal Welfare]
Handbook on the Care and Management of Laboratory Animals Seventh
Edition Poole T, English P (eds ), 21-27. Blackwell Science,
Oxford
Very helpful discussion of positive reinforcement training
for cooperation during procedures. "By making the shift to
a more positive reinforcement-based system, the welfare of the
animals is significantly enhanced while providing better (less
stressed) research models for the biomedical community."
T-W-Fiennes RN 1972. Primates - General.
In The UFAW Handbook on the Care and Management of Laboratory
Animals Fourth Edition UFAW [Universities Federation for Animal
Welfare] (ed), 374-375. Churchill Livingstone, London
"The higher primates, such as chimpanzees and baboons,
are intelligent and sensitive. If handled with sympathy and understanding
they can become more than research tools - even cooperative partners
in experimentation. To achieve this, a little time, often time
well spent, must be spent on conditioning the animals. A chimpanzee,
for instance, will sit quietly and hold his arm out for a blood
sample to be taken. ... An animal treated unsympathetically is
liable to become aggressive and uncooperative; furthermore, unless
care is taken over its comfort and needs, it is liable to become
stressed and the results of the experiment may be vitiated for
this reason."
(3,2) Species-specific Recommendations
Baboons (Papio spp.)
Levison PK, Fester CB, Nieman WH,
Findley JD 1964. A method for training unrestrained primates to
receive drug injection. Journal of the Experimental Analysis
of Behavior 7, 253-254
Training technique by which an adult, single-housed male baboon
learned to offer his arm through a pothole and accept intramuscular
injection in this home cage is described and the result demonstrated
with a photo. Injection was reliably obtained after approximately
nine one-hour training sessions.
Turkkan JS, Ator NA, et al
1989. Beyond chronic catheterization in laboratory primates. In
Housing, Care and Psychological Well-being of Captive and Laboratory
Primates Segal EF (ed), 305-322. Noyes Pub, Park Ridge
Training protocols are described to ensure cooperation of single-housed
baboons during blood pressure measurement and during oral drug
dosing in the homecage.
Chimpanzees (Pan troglodytes)
Bloomsmith MA, Laule GE, Alford PL,
Thurston RH 1994. Using training to moderate chimpanzee aggression
during feeding. Zoo Biology 13, 557-566
"Positive reinforcement training techniques were applied
to reduce a dominant male chimpanzee's aggression and chasing
during meals. Verbal commands and food reinforcers were used to
train him to sit and remain seated while other group members received
and ate their share of produce."
Bloomsmith MA, Stone AM, Laule GE
1998. Positive reinforcement training to enhance the voluntary
movement of group-housed chimpanzees within their enclosure. Zoo
Biology 17, 333-341
"Positive reinforcement techniques were applied to train
groups of chimpanzees to move voluntarily into the indoor portions
of their enclosures at the request of trainers and to be briefly
restricted to those areas."
Kessel-Davenport AL, Gutierrez T 1994.
Training
captive chimpanzees for movement in a transport box. The
Newsletter 6(2), 1-2
Training technique is described. "Thirty-seven [group-housed]
captive chimpanzees were trained using operant conditioning to
enter a transfer box." [Age and sex of subjects is not provided.]
Lambeth SP, Perlman JE, Schapiro SJ
2000. Positive reinforcement training paired with videotape exposure
decreases training time investment for a complicated task in female
chimpanzees. American Journal of Primatology 51(Supplement
1), 79-80
"Five females were exposed to a 10-minute videotape of
female chimpanzees being positively reinforced for successfully
urinating into a cup. Immediately following videotape exposure,
these subjects participated in a training session." On average
experimental and control subjects received 56 minutes of training.
"Subjects with videotape exposure successfully responded
to the command to urinate in significantly less time than did
controls."
Laule GE, Thurston RH, Alford PL,
Bloomsmith MA 1996. Training to reliably obtain blood and urine
samples from a diabetic chimpanzee (Pan troglodytes). Zoo
Biology 15, 587-591
Training techniques are described to gain the cooperation of
a 3-year old female chimpanzee in obtaining blood and urine samples.
"The first blood draw occurred during the 18th training session,
with a total of 275 minutes invested prior to that. The first
successful [urine] collection occurred in session 4 in less than
4 min after a total of 42 min of training time."
Laule G 1999 Training laboratory animals.
In The UFAW Handbook on the Care and Management of Laboratory
Animals Seventh Edition Poole T, English P (eds ), 21-27.
Blackwell Science, Oxford
Very helpful discussion of positive reinforcement training
for cooperation during procedures. "By making the shift to
a more positive reinforcement-based system, the welfare of the
animals is significantly enhanced while providing better (less
stressed) research models for the biomedical community."
Perlman JE, Thiele E, Whittaker MA,
Lambeth SP, Schapiro SJ 2004. Training
chimpanzees to accept subcutaneous injections using positive reinforcement
training techniques. American Journal of Primatology 62(Supplement),
96
”Positive reinforcement training techniques were used to
train four socially-housed, adult chimpanzees to present their
abdomen for a subcutaneous injection. .. Subjects had been previously
trained to present body parts for inspection, including the abdomen.
For the present study, subjects were trained to 1) present the
abdomen, 2) tolerate a pinch of the skin, 3) accept the subcutaneous
insertion of a needle, and 4) remain stationary while the contents
of the syringe were injected. Three of the four chimpanzees were
reliably trained to voluntarily accept the subcutaneous injection.
A mean of 98 minutes of training time was required for the animals
to reliably accept penetration and injection of up to 10 cc through
a 25-gauge needle. Training sessions lasted 5 to 8 minutes and
13 - 20 sessions (mean = 17) were required to achieve reliable
performance.“
Russell JL, Taglialatela JP, Hopkins WD 2006. The use of positive
reinforcement training in chimpanzees (Pan troglodytes)
for voluntary presentation for IM injections. American Journal
of Primatology 68(Supplement ), 122 (Abstract)
"Positive reinforcement has been used to gain the cooperation
of captive primates for research and management needs. In this
study, ten chimpanzees .. were trained to present for intramuscular
(IM) injections. Clicker training was used to teach subjects to
present their leg and accept an injection. .. Subjects reached
criterion for presenting for a touch from a needle in 7 to 44
training sessions. .. These results suggest that through the use
of positive reinforcement, chimpanzees can be quickly and reliably
trained to present for injections as part of a research protocol
requiring multiple accesses."
Schapiro SJ, Perlman JE, Thiele E,
Lambeth S 2005. Training nonhuman primates to perform behaviors
useful in biomedical research. Lab Animal 34(5), 37-42
Training protocols are described and the time investments to
achieve cooperation for semen collection [7 subjects: 29-453 minutes],
subcutaneous [2 subjects: 90-104 minutes; 1 subject could not
be trained] and intramuscular injection [39 subjects: 0.1-396
minutes; 43 subjects could not be trained] are presented.
Spragg SDS 1940. Morphine addiction
in chimpanzees. Comparative Psychology Monographs 15, 1-132
Author provides formal description of training four unrestrained
chimpanzees to approach an investigator and accept an injection
of physiological saline solution. The training comprised a combination
of adaptation, desensitization, and shaping, with fruit, praise,
and patting as reinforcers. "It is the writer's contention
that this preliminary adaptation to the injection situation was
an important factor for the experiment; it obviated many undesirable
aspects which would have appeared if it had been necessary to
inject the animals by force."
Videan EN, Fritz J, Murphy J, Borman
R, Smith HF, Howell S 2005. Training captive chimpanzees to cooperate
for an anesthetic injection. Lab Animal 34(5), 43-48
Training protocol is described in detail and the time investment
presented.
Videan EN, Fritz J, Murphy J, Howell S, Heward CB 2005. Does
training chimpanzees to present for injection lead to reduced
stress? Laboratory Primate Newsletter 44(3), 1-2
"Subjects were 17 captive chimpanzees living at the
Primate Foundation of Arizona, aged 10.6 to 34.5 years at the
time of the study. The sample included 8 males and 9 females.
Eleven of the subjects were trained, using positive reinforcement
techniques, over 21 months (Videan et al., 2005). Individuals
were trained to present an arm or leg to the cage mesh for anesthetic
injection, using the verbal cues "arm" and "leg".
Training procedures were transferred from the trainer to either
the colony manager or the assistant colony manager, after behaviors
were under stimulus control, in 5 of the trained subjects. ..
When all trained individuals were pooled, trained subjects exhibited
significantly lower levels of cortisol than untrained (U=7, p<0.010,
Table 1)."
Drills (Mandrillus spp.)
Priest GM 1991. Loon, the Diabetic
Drill (Videotape) Mac & Mutley, San Francisco
Training technique for in-homecage blood collection of an adult
male drill is clearly demonstrated.
Priest GM 1991. The methodology for
developing animal behavior management programs at the San Diego
Zoo and Wild Animal Park. American Zoo and Aquarium Association
(AZA) Annual Conference Proceedings, 553-562
"Within a few weeks, Loon was voluntarily allowing the
veterinarians to draw blood from his forearm. Loon has voluntarily
accepted his daily insulin injections and blood withdrawals for
over two years."
Gorillas (Gorilla spp.)
Bettinger T, Kuhar C, Sironen A, Laudenslager
M 1998. Behavior and salivary cortisol in gorillas housed in an
all male group. American Zoo and Aquarium Association (AZA)
Annual Conference Proceedings, 242-246
Gorillas were successfully trained to voluntarily chew on the
cotton plugs then return them to the caretaker.
Bond M 1991. How to collect urine
from a gorilla. Gorilla Gazette 5(3), 12-13
Training technique is clearly described. Mandara "not
only urinates on demand but has been known to go get a drink of
water if we happen to ask for a sample when her bladder is empty."
Brown CS 1997. Training gorillas (Gorilla
gorilla gorilla) for noninvasive semen collection. Proceedings
American Association of Zoo Veterinarians, 201-203
"Appropriate behaviors, in response to verbal prompts,
were rewarded with praise and food treats. Collection of the first
semen sample [from single-housed subjects] varied from 5-14 months
after the initiation of training, with collections occurring earliest
on the animal that appeared to have the best relationship with
the trainer."
Brown CS 1998 A Training Program
for Semen Collection in Gorillas (Videotape). Henry Doorly
Zoo, Ohama
Training technique to ensure cooperation of single-housed adult
male gorillas during physical examination, injection, semen collection
are described and very clearly demonstrated.
Segerson L, Laule GE 1995. Initiating
a training program with gorillas at the North Carolina Zoological
Park. American Zoo and Aquarium Association (AZA) Annual Conference
Proceedings, 488-489
Technique is clearly described to facilitate wound treatment
of an unrestrained, single-housed female gorilla.
Macaques (Macaca spp.)
*Baumans V, Coke
C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,
Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals
in Research Labs - Chapter
7.2. Injection and Blood Collection--How to minimize Stress Reactions.
Washington, DC: Animal Welfare Institute
"With positive reinforcement, I have trained adult female
cynos to cooperate during intramuscular injection in home cages
that are not equipped with squeeze-backs. When they can
trust you, they readily learn to cooperate during this common
procedure. These animals work with rather than against me, which
automatically implies that they show no fear or stress reactions
during the procedure."
Bunyak SC, Harvey NC, Rhine Rj, Wilson
MI 1982. Venipuncture and vaginal swabbing in an enclosure occupied
by a mixed-sex group of stumptailed macaques (Macaca arctoides).
American Journal of Primatology 2, 201-204
By the end of five training sessions "it was no longer
necessary to net and restrain the females. Indeed, some of the
females began voluntarily to approach the researcher and present
for vaginal swabbing."
Clarke MR, Phillippi KM, Falkenstein
JA, Moran EA, Suomi SJ 1990. Training Corral-living Rhesus
Monkeys for Fecal and Blood Sample Collection (Videotape).
Delta Primate Research Center, Covington
Training technique is explained and the animals' reactions
demonstrated.
Down N, Skoumbourdis E, Walsh M, Francis
R, Buckmaster C, Reinhardt V 2005. Pole-and-collar
training: A disucssion by the Laboratory Animal Refinement and
Enrichment Forum. Animal Technology and Welfare 4,
157-161
Experiences with the pole-and-collar training training
are shared. "Yes, most monkeys can be trained but some cannot,
or let's say they should not be trained because their personality
hich is presumably conditioned through negative experiences with
people is very difficult to deal with."
Friscino BH, Gai CL, Kulick AA, Donnelly
MJ, Rockar RA, Aderson LC, Iliff SA 2003. Positive reinforcement
training as a refinement of a macaque biliary diversion model.
AALAS [American Association for Laboratory Animal Science]
54th National Meeting Official Program, 101
"Animals that adapted to wearing jackets were surgically
implanted with a biliary diversion cannula system, a venous cannula
and three subcutaneous access ports. .. The animals [three females
and nine male rhesus] were trained to present the pouch and to
remain stationary while the catheters were accessed. The length
of time required for training was variable between individuals,
but generally required three to four training sessions during
a two-week period. These in-cage procedures precluded the need
for chair or manual restraint of animals during sample collection.
Instead, positive reinforcement was used to reward the animals
with food for their cooperation during sample collection. This
has also increased the efficiency of conducing metabolic studies
and minimized the potential stress of sample collection for both
the personnel and animals."
Goodwin J 1997. The application, use, and effects of training
and enrichment variables with Japanese snow macaques (Macaca
fuscata) at the Central Park Wildlife Center. American
Zoo and Aquarium Association (AZA) Regional Conference Proceedings,
510-515
Training protocol is briefly described which allows the keepers
through vocal and visual cues to herd the animals to a holding
area.
Heath M 1989. The
training of cynomolgus monkeys and how the human/animal relationship
improves with environmental and mental enrichment. Animal
Technology 40(1), 11-22
"A relatively short, but predictable, course of routine
handling and feeding enabled the monkeys to co-operate with their
handlers and made working practices a lot easier, quicker and
safer for both the animals and technicians."
Luttrell L, Acker L, Urben M, Reinhardt
V 1994. Training
a large troop of rhesus macaques to cooperate during catching:
Analysis of the time investment. Animal Welfare 3,
135-140
"Using a simple chute system and applying a training technique
based on patience, all 45 troop members were successfully conditioned
in less then 15 work-hours to voluntarily enter a transport cage
one by one."
Phillippi-Falkenstein K, Clarke MR
1992. Procedure for training corral-living rhesus monkeys for
fecal and blood-sample collection. Laboratory Animal Science
42, 83-85
Clear description of training technique. "By day 9, the
male stopped resisting, and three of the [five] females extended
their legs voluntarily."
Reinhardt V 1990. Avoiding
undue stress: Catching individual animals in groups of rhesus
monkeys. Lab Animal 19(6), 52-53
Training technique is described. "We have successfully
trained two heterogeneous rhesus troops of 28 and 33 members.
The catching procedure has become a routine that is no longer
associated with excitation and distress. It is now possible for
one experienced person to catch animals at any given time without
extra help."
Reinhardt V 1990. Catching Individual
Rhesus Monkeys Living in Captive Groups (Videotape). Available
on loan from Animal Care Audio-Visual Materials, WRPRC, 1220 Capitol
Court, Madison, WI 53715
Using vocal commands, a single person swiftly catches all members
of a trained rhesus breeding group one-by-one in a transport cage
without causing any disturbance or stress.
Reinhardt V 1996. Refining
the blood collection procedure for macaques. Lab Animal
32(1), 32-35
A training technique is described for ensuring the active cooperation
of pair-housed/single-housed adult male and female rhesus and
stump-tailed macaques during in-homecage venipuncture. Mean cumulative
training time investment per individual was less than one hour.
The training eliminated significant cortisol responses which typically
occur during conventional, i.e., enforced blood collection.
Reinhardt V, Cowley D 1990. Training
stumptailed monkeys to cooperate during in-homecage treatment.
Laboratory Primate Newsletter 29(4), 9-10
One to 14 training sessions, each lasting for 1-5 minutes,
were required to train adult, pair-housed and single-housed stump-tailed
macaques of both sexes to cooperate during topical treatment in
the homecage.
*Skoumbourdis
EK 2008. Pole-and-collar-and-chair training. Laboratory Animal
Refinement & Enrichment Forum (electronic discussion group)
, January 24, 2008
http://groups.yahoo.com/group/LAREF/members
"All the monkeys I have pole/collar/chair trained have
gone through an initial phase of resistance both when the pole
was being attached to the collar, and when they were first put
into the chair, but for the most part they finally did settle
down and cooperate. All it takes is patience and gentle determination
on the part of the trainer.
Trust in the trainer is the ultimate key for success. Nonhuman
primates are intelligent; when they are free of apprehension or
fear, they quickly figure out that it is much easier and even
rewarding for them to cooperate with you rather than resist. A
successfully trained monkey will have developed so much trust
in you that he/she will never fight against you when you pole
and chair him/her.
To pole-collar-chair train a monkey can be a very rewarding process
that is not necessarily time-consuming. I have successfully trained
19 animals:
two adult female rhesus, four adult male rhesus, five juvenile
male rhesus, four adult female cynomolgus, and four adult male
cynomolgus.
My quickest subject took just five days of training to reliably
cooperate (I should mention that he was two years old and an angel!),
while other animals have taken me well over a month to get going
especially older rhesus who can be very stubborn and hard to food-motivate.
Also, I have had some animals who were just never meant to be
put in a chair. This is a reality that both you and the investigators
must acknowledge. You cannot force a monkey to cooperate and be
relaxed in the chair. It's impossible. Sure, you can try, but
you're not going to win."
Marmosets (Callithrix spp.)
Anzenberger G, Gossweiler H 1993.
How to obtain individual urine samples from undisturbed marmoset
families. American Journal of Primatology 31, 223-230
"An apparatus and a method are described, which allow
simultaneous urine collection from all individual members of undisturbed
marmoset families. By the end of the third week of training, it
was not unusual to collect urine samples from an entire family."
McKinley J, Buchanan-Smith HM, Bassett
L, Morris K 2003. Training common marmosets (Callithrix jacchus)
to cooperate during routine laboratory procedures: Ease of training
and time investment. Journal of Applied Animal Welfare Science
6, 209-220
Behaviours taught were target training to allow in homecage weighing
and providing urine samples from 12 pairs of marmosets. "Between
2 to 13, 10-minute training sessions established desired behaviors.
.. Trained animals proved extremely reliable, and data collection
using trained animals was considerably faster than collection
using current laboratory techniques."
Smith TE, McCallister JM, Gordon SJ,
Whittikar M. 2004. Quantitative data on training new world primates
to urinate. American Journal of Primatology 64(1), 83-93
"This study assessed the effectiveness of operant conditioning
in training three species of captive callitrichid primates (Leontopithecus
rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate
on demand...Training sessions (30 min each) were conducted at
dawn thrice weekly during five consecutive phases: habituation,
control, training (animals were rewarded for urinating), maintenance
(animals had reached a defined training criteria and continued
to be rewarded for urinating), and collection (animals were rewarded
for urinating, and the trainer entered the cage to collect the
sample). The numbers of 30-min training sessions required to train
the three monkey species (L. rosalia, C. geoffroyi, and S. imperator)
were five, six, and eight, respectively. For the three species,
the mean number of urinations per animal was significantly greater
during the training, maintenance, and collection phases compared
to the control phase... The entry of the trainer into the cage
to collect the urine sample did not appear to alter urination
behavior. We demonstrate that operant conditioning techniques,
which typically incur minimal cost, time investment, and disturbance,
can be used to increase the quantity of urine samples collected
for physiological analysis, the proportion of animals that urinate,
and the speed of sample collection."
Orangutans (Pongo pymgmaeus)
Berman N, Greenblatt H 1989. Training
Medical Behaviors in Orangutans at Brookfield Zoo (Videotape).
Chicago Zoological Society, Chicago
Training technique is clearly described and demonstrated to
ensure cooperation of two pair-housed female/male orangutans during
daily insulin injection.
Moore BA, Suedmeyer K 1997. Blood
sampling in 0.2 Bornean orangutans at the Kansas City Zoological
Gardens. Animal Keepers' Forum 24, 537-540
Training technique is clearly described to ensure cooperation
during in-homecage blood collection of adult, pair-housed female
orangutans.
Sakis (Pithecia spp.)
Shideler SE, Savage A, Ortuño
AM, Moorman EA, Lasley BL 1994. Monitoring female reproductive
function by measurement of fecal estrogen and progesterone metabolites
in the white-faced saki (Pithecia pithecia). American
Journal of Primatology 32, 95-108
"Fist morning void urine was collected directly in a polypropylene
container hand-held under the female subject. A second container
was held under the female to collect fecal material. [The group-housed]
females urinated and defecated within 5-20 min. Following sample
collection, females were rewarded for their cooperation with more
sunflower seeds."
Spider monkeys (Ateles goeffroyi)
Hernándes-López L, Mayagoitia
L, Esquivel-Lacroix C, Rojas-Maya S, Mondragón-Ceballos
R 1998. The menstrual cycle of the spider monkey (Ateles geoffroyi).
American Journal of Primatology 44, 183-195
Four of the five females were trained to enter a small cage
attached to the door of their enclosure and to "allow a cotton
swab to be introduced in the vagina. This procedure was slightly
modified [not described], and the animals were trained to be injected
with ketamine" for subsequent blood collection.
Squirrel monkeys (Saimiri spp.)
Panneton M, Alleyn S, Kelly N 2001.
Chair restraint for squirrel monkeys. 2001 AALAS [American
Association for Laboratory Animal Science] Official Program,
92
"Commonly used procedures include moveable-back cages,
manual restraint and the use of restraint chairs. Such procedures
have the potential to cause emotional distress to the animals
due to adverse conditioning. ... Our facility has trained squirrel
monkeys to cooperate during various procedures such as capture
from their homecage and chair restraint for periods not exceeding
1 h. ... Each squirrel monkey [in the chair] is constantly supervised
and given positive reinforcement during and after the training
sessions. ... The initial training [habituation] period starts
at 5-10 min three times a week. Additional training sessions of
5-20 min are added until 1 h of chair restraint is achieved. At
this time, training is reduced to twice a week for 1 h and then
once a week for maintenance. ... Concerns such as weight loss,
chair abrasions and hypglycemia are among some of the obstacles
to overcome."
Tamarins (Saguinus spp.)
Snowdon CT, Savage A, McConnell PB
1985. A breeding colony of cotton-top tamarins (Saguinus oedipus).
Laboratory Animal Science 35, 477-480
Group-housed females were conditioned to urinate into containers
each morning in return for a food reward.
Smith TE, McCallister JM, Gordon SJ,
Whittikar M. 2004. Quantitative data on training new world primates
to urinate. American Journal of Primatology 64(1), 83-93
"This study assessed the effectiveness of operant conditioning
in training three species of captive callitrichid primates (Leontopithecus
rosalia, Callithrix geoffroyi, and Saguinus imperator) to urinate
on demand...Training sessions (30 min each) were conducted at
dawn thrice weekly during five consecutive phases: habituation,
control, training (animals were rewarded for urinating), maintenance
(animals had reached a defined training criteria and continued
to be rewarded for urinating), and collection (animals were rewarded
for urinating, and the trainer entered the cage to collect the
sample). The numbers of 30-min training sessions required to train
the three monkey species (L. rosalia, C. geoffroyi, and S. imperator)
were five, six, and eight, respectively. For the three species,
the mean number of urinations per animal was significantly greater
during the training, maintenance, and collection phases compared
to the control phase... The entry of the trainer into the cage
to collect the urine sample did not appear to alter urination
behavior. We demonstrate that operant conditioning techniques,
which typically incur minimal cost, time investment, and disturbance,
can be used to increase the quantity of urine samples collected
for physiological analysis, the proportion of animals that urinate,
and the speed of sample collection."
Vervet monkeys (Cercopithecus aethiops)
*Baumans V, Coke
C, Green J, Moreau E, Morton D, Patterson-Kane E, Reinhardt A,
Reinhardt V, Van Loo P 2007 Making Lives Easier for Animals
in Research Labs - Chapter
7.3. Oral Drug Administration. How to minimize Stress Reactions.
Washington, DC: Animal Welfare Institute
"Our vervet monkeys voluntarily swallow drugs when we
mix these with their regular diet, consisting on pre-cooked maize,
fortified with vitamins, minerals and other ingredients. The dry
ingredients are blended with water and form a stiff putty-like
paste, which is an ideal vehicle for mixing in test substances.
If the flavor needs to be masked, there are a variety of possibilities,
such as honey and syrup, depending on what the protocol permits.
We usually administer the compound in about a third of the morning
feed. The bulk of the food is offered after this portion has been
consumed. Some substances we even mix into the entire bulk of
the morning feed. Keeping the compound too long in cheek pouches
or spitting it out has never been a problem. We have used this
simple oral administration technique for pharmacokinetic studies
very successfully. Over a time period of 20 years, we have not
had to deal with any substance that we could not feed to the vervets,
including bitter herbal mixtures in fairly high concentrations."
Kelley TM, Bramblett CA 1981. Urine
collection from vervet monkeys by instrumental conditioning. American
Journal of Primatology 1, 95-97
Training technique is described. Six of eight group-housed
males reliably produced clean urine samples after a two-month
period of training.
Woolly monkeys (Lagothrix spp.)
Logsdon S 1995. Use of operant conditioning
to assist in the medical management of hypertension in woolly
monkeys. American Zoo and Aquarium Association (AZA) Regional
Conference Proceedings, 96-102
Training technique is described. "Currently, two monkeys
[one adult female and one adult male] have had their blood pressure
measured in the group without being restrained."
(4) Promoting Foraging and Food Processing Behavior