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to Table of ContentsBibliography on Refinement and Environmental Enrichment for Primates. Refinement
(1) Definition
(2,a) Unstructured
Space
(2,b) Structured Space
(2,c) Playpen, Outdoor
Housing, Exercise Cage
(3) Inanimate
Enrichment
(4) Acoustical
Enrichment
(5) Animate Enrichment
(6) Natural
Weaning
(7) Working
with Cooperative Animals
(8) Treatment
of Trained Animals in their Home Enclosure
(9) Cage Arrangement
Refinement is the attempt to enhance animal welfare and control extraneous variables that may increase research data variability.
Bayne K, McCully C 1989. The effect
of cage size on the behavior of individually housed rhesus monkeys.
Lab Animal 18(1), 25-28
A moderate increase of unstructured cage space does not affect
stereotypical behaviors in individually caged rhesus macaques
Boot R, Leussink AB, Vlug RF 1985.
Influence of housing conditions on pregnancy outcome in cynomolgus
monkeys (Macaca fascicularis). Laboratory Animal Science
19, 42-47
More successful pregnancies were recorded for females housed
individually in large cages than for females housed in small cages.
Brent L 1992. The effects of cage
size and pair housing on the behavior of captive chimpanzees.
American Journal of Primatology 27, 20
"Environmental manipulation was higher and inactivity
lower in the [furnished] large single cage than in the [furnished]
small single cage. The mean abnormal behaviors decreased in the
larger cages but the difference was not significant."
Crockett CM, Shimoji M, Bowden DM
2000. Behavior, appetite, and urinary cortisol responses by adult
female pigtailed macaques to cage size, cage level, room change,
and ketamine sedation. American Journal of Primatology 52, 63-80
A moderate increase of unstructured cage space does not affect
abnormal behaviors in individually caged pig-tailed macaques.
Daschbach NJ, Schein MW, Haines DE
1983. Cage-size effect on locomotor, grooming and agonistic behaviors
of the slow loris (Nycticebus coucang). Applied Animal
Ethology 9, 317-330
"Results of the experiments in this study indicate that
slow lorises kept in larger [furnished] cages will be more active
than those housed in [furnished] cages approaching recommendations
for size proposed by the U.S. National Research Council."
Kitchen AM, Martin AA 1996. The effects
of cage size and complexity on the behaviour of captive common
marmosets, Callithrix jacchus jacchus. Laboratory Animals
30, 317-326
"Stereotyped behaviours, which occurred in the small [furnished]
cages, were never exhibited in the large [furnished] cages. We
conclude that the welfare of captive marmosets is enhanced by
the provision of larger and more complex cages."
Line SW, Morgan KN, Markowitz H, Strong
S 1990. Increased cage size does not alter heart rate or behavior
in female rhesus monkeys. American Journal of Primatology
20, 107-113
A moderate increase of the dimensions of standard cages that lack
any structures for climbing, perching, swinging or other activities
did not affect the behavior of individually caged rhesus macaques.
Mallapur A, Waran N, Sinha A 2005.
Use of enclosure space by captive lion-tailed macaques (Macaca
silenus) housed in Indian zoos. Journal of Applied Animal
Welfare Science 8, 175-185
"Captive lion-tailed macaques used the edge zone the space
closest to the visitor areas when their ... environments were
deficient in appropriate environmental stimuli."
Paulk HH, Dienske H, Ribbens LG 1977.
Abnormal behavior in relation to cage size in rhesus monkeys.
Journal of Abnormal Psychology 86, 87-92
"Observations were made of 24 monkeys that were introduced
singly into a [barren] small and a [barren] large test cage. In
a large cage, more normal but less stereotyped locomotion was
shown than in a small cage."
Williams LE, Steadman A, Kyser B 2000.
Increased cage size affects Aotus time budgets and partner
distances. American Journal of Primatology 51(Supplement
1), 98
"Aotes spp. housed in typical, small, laboratory cages
appear to be sedentary animals that spend large amounts of time
sitting alone or in physical contact with social partners. ...
The Aotus, housed as pairs or family groups, were moved from cages
measuring 0.63m x 1.5m x 0.76m to larger housing measuring 1.5m
x 3m x 2m. Perches and nest boxes were provided in both housing
conditions. ... Results indicate that Aotus will disperse and
use the cage area provided. Changes in time budgeting are indicative
of more relaxed animals, spending less time huddled with family
members or in their nest box [alone], and spending more time eating
and drinking."
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."
Günther MM 1998. Influence of
habitat structure on jumping behaviour in Galago moholi.
Folia Primatologica 69(Supplement 1), 410
"These results suggest that support material [perches],
as well as height, influences the behaviour of G. maholi and these
should be taken into consideration in behavioural and biomedical
studies as well as in the construction of cage facilities. Studies
which do not take these factors into account are to some extent
vitiated."
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."
McCormack K, Megna NL 2001. The effects of privacy walls on aggression
in a captive group of rhesus macaques (Macaca mulatta). American Journal of Primatology 54(Supplement
1), 50-51
"Preliminary results suggest that non-contact aggression
(vocalizations, fear grimaces, chases, and threats) is significantly
reduced after the introduction of the privacy walls (p<.05)."
Miller-Schroeder P, Paterson JD 1989.
Environmental influences on reproduction and maternal behavior
in captive gorillas: Results of a survey. In Housing, Care
and Psychological Wellbeing of Captive and Laboratory Primates
Segal EF (ed), 389-415. Noyes Publications, Park Ridge
Females reproduced more successfully if their enclosures contained
various structures, especially privacy refuges like sight barriers
and cages.
Nakamichi M, Asanuma K 1998. Behavioral
effects of perches on group-housed adult female Japanese monkeys.
Perceptual and Motor Skills 87, 707-714
"When [4 adult female] monkeys were housed in a cage which
contained eight wooden perches to increase usable space, the rate
of agonistic interactions ... decreased in comparison with those
evident when they were housed in a cage [identical dimension]
without such perches."
National Research Council 1998. The
Psychological Well-Being of Nonhuman Primates NAP, Washington
http://pompeii.nap.edu/books/0309052335/html/index.html
"Optimal use of available cage space might well depend
more on the placement of perches, platforms, moving and stationary
supports, and refuges than on cage size itself."
Neveu H, Deputte BL 1996. Influence
of availability of perches on the behavioral well-being of captive,
group-living mangabeys. American Journal of Primatology
38, 175-185
"A total deprivation of perches yielded an increase in
aggressive behaviors and locomotion, and a decrease in cohesiveness.
Placing perches progressively in the experimental cage restored
the level of all the variables to levels found in the control
cage [with five perches]."
Reinhardt V 1989. Evaluation
of the long-term effectiveness of two environmental enrichment
objects for singly caged rhesus macaques. Lab Animal
18(6), 31-33
"While perching, the monkeys sat in front of the cage
for 95% of the time, in the middle or rear of the cage for 5%
of the time. ... The proportion of time spent with the pipes was
three times greater for animals living in lower-row cages than
for animals living in upper-row cages. ... In the elevated position,
the light exposure was increased, a fact that made the pipes of
particular value for the lower-row cages animals."
Reinhardt V 1990. A
perch for caged macaques. Humane Innovations and Alternatives
in Animal Experimentation 4, 134-135
Perches are "particularly attractive for animals during
the daily cleaning of their cages because they offer a dry, comfortable
place to sit while the floors of their cages are sprayed with
water."
Ricker RB, Williams LE, Brady AG,
Gibson SV, Abee CR 1995. Environmental enhancement for laboratory-housed
squirrel monkeys: Fifteen-year retrospective analysis of procedures.
Contemporary Topics in Laboratory Animal Science 34(4),
55
"Cut pieces of PVC pipe (12 in diameter) were hung in
each run as a hide box, allowing eye contact to be broken between
disputing animals. This decreased fight wounds by 60%."
Shimoji M, Bowers CL, Crockett CM
1993. Initial response to introduction of a PVC
perch by singly caged Macaca fascicularis. Laboratory Primate Newsletter 32(4),
8-11
Single-housed "monkeys spent significantly more time clinging
to the cage wall ("suspended") in the absence of the
perch. ... There was less stereotypy when the perch was present."
Spencer H 2005. A tale of two cynos.
Tech Talk 10(3), 4 & 6
"After implementing the vertical tunnels, both [pair-housed
male cynos] primates stopped exhibiting stereotypical and self-injurious
behaviors." The two animals "were free of stereotypical
behavior for a little over two years."
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
"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."
Wolff A 1989. Polyvinyl
chloride piping as perch material for squirrel monkeys. Laboratory
Primate Newsletter 28(1), 7
"An additional unexpected benefit of the PVC piping has
been a decrease in dorsal tail-head abrasions, frequently seen
in squirrel monkeys that sit on the stainless steel flooring of
standard primate cages."
(2,c) Playpen, Outdoor Housing, Exercise Cage
Baker KC, Ross SK 1998. Outdoor access:
The behavioral benefits to chimpanzees. American Journal of
Primatology 45, 166
"When compared to the results of ameliorative environmental
enrichment techniques furnished to the indoor-housed subjects,
the small outdoor groups of [two or three] chimpanzees showed
broader and more dramatic improvements in well-being." Animals
with outdoor access showed significantly less abnormal behavior
(e.g., coprophagy, regurgitation/reingestion), less yawning, and
more self-grooming.
Bayne K, Dexter S, Suomi S 1992. A
preliminary survey of the incidence of abnormal behavior in rhesus
monkeys (Macaca mulatta) relative to housing condition.
Lab Animal 21(5), 38-46
"The greatest frequency of overall abnormal behavior and
stereotypic exploratory behavior was in the SC [single cage] condition,
and the lowest frequency of occurrence in the CC [corn crib] condition
... in IO [indoor/outdoor] runs, the animals showed no self-directed
behavior."
Brent L, Lee DR, Eichberg JW 1991.
Evaluation
of a chimpanzee enrichment enclosure. Journal of Medical
Primatology 20, 29-34
Chimpanzees were given access to a complex new outdoor playground.
"Activity and environmental manipulation increased while
abnormal and self directed behaviors decreased."
Bryant CE, Rupniak NMJ, Iversen SD
1988. Effects
of different environmental enrichment devices on cage stereotypies
and autoaggression in captive cynomolgus monkeys. Journal
of Medical Primatology 17, 257-269
"Stereotypy and autoaggression were markedly reduced in
the playpen, but reappeared on return to the home cage."
Clarke AS, Juno CJ, Maple TL 1982.
Behavioral effects of a change in the physical environment: a
pilot study of captive chimpanzees. Zoo Biology 1, 371-380
A group of chimpanzees was translocated from a laboratory environment
to a naturalistic man-made island. Stereotyped and self-directed
behaviors were dramatically reduced on the island.
Fontenot MB, Wilkes MN, Lynch CS 2006. Effects of outdoor housing
on self-injurious and stereotypic behavior in adult male rhesus
macaques (Macaca mulatta). Journal of the American Association
for Laboratory Animal Science [Contemporary Topics in Laboratory
Animal Science] 45(5), 35-43
"Our findings suggest that self-biting and self-directed
stereotypic behavior in rhesus macaques with a history of self-injurious
behavior is significantly reduced by outdoor housing" in
corncribs equipped with perches and toys. The outdoor housing
provided a 114% increase in floor area for single-housed animals
and a 364% to 837% increase in floor area for group-housed animals.
Fried J, Whitehouse M 1992. A pre-post
occupancy comparison of activity budgets and habitat utilization
in a group of captive mandrills (Mandrillus sphinx). American
Journal of Primatology 27, 28
"For the group as a whole, feeding, traveling and object
oriented behaviors increased, and stereotypic behaviors decreased"
in the naturalistic environment.
Goerke B, Fleming L, Creel M 1987.
Behavioral changes of a juvenile gorilla after a transfer to a
more naturalistic environment. Zoo Biology 6, 283-295
"Coprophagy and regurgitation/reingestion were reduced
in the juvenile [group-housed] gorilla in the larger and more
natural environment."
Honess PE, Marin C, Brown AP, Wolfensohn
SE 2005. Assessment of stress in non-human primates: application
of the neutrophil activation test. Animal Welfare 14, 291-295
"All macaques were group-housed indoors in either a traditional
caging system of three linked modules of typical reinforced stainless
steel two-tier laboratory cages, or in open-rooms containing either
these cages with the fronts removed or no caging at all. ... Animals
housed in a traditional caging system produced a significantly
lower leukocyte response than animals housed in open-rooms, indicating
that there was a higher level of stress associated with caged
housing than open-room housing."
Jensvold MLJ, Fouts RS, Fouts DH 1999.
Behavioral changes in captive chimpanzees. ChimpanZoo Conference
Proceedings, 66
"Overall, after the move to the larger [structurally enriched]
facility, there was an increase in activity, a decrease in stereotypical
behaviour, and an increase in threat behavior."
Kessel AL, Brent L 1995. An activity
cage for baboons, Part I. Contemporary Topics in Laboratory
Animal Science 34(6), 74-79
Single-housed "baboons provided with a large enriched
activity cage [during two days each month] display dramatic changes
in behavior typically considered to represent positive psychological
well-being. ... The home cages and the activity cage were located
in the same room, and provided visual, olfactory, and auditory
access to other baboons." .
Kessel AL, Brent L 1997. Behavioural
effects of transferring singly housed baboons to outdoor social
groups. In Proceedings on the 2nd International Conference
on Environmental Enrichment Holst B (ed), 142-147. Copenhagen
Zoo, Frederiksberg
"Moving singly housed baboons to an enriched outdoor enclosure
had significant effects on all behaviors analyzed. Abnormal behavior,
cage directed activities, and self-directed activities all decreased
in the corn cribs. Inactivity, locomotion, and normal behavior,
as well as enrichment directed activities and social behavior
all increased in the corn cribs."
Leu M, Crockett CM, Bowers CL, Bowden
DM 1993. Changes in activity levels of singly housed longtailed
macaques when given the opportunity to exercise in a larger cage.
American Journal of Primatology 30, 327
"Over a period of 36 days, each [single-housed] animal
had 15 min per day access to a multicompartmental [large] exercise
cage." Locomotion increased while stereotypical behavior
decreased when the animals were in the exercise cage.
Maple TL, Finlay TW 1987. Post-occupancy
evaluation in the zoo. Applied Animal Behaviour Science
18, 5-18
"We investigated the effects of translocating great apes
from barren cages to innovative naturalistic habitats. ... For
both gorillas and orangutans, the new environment had the effect
of reducing the variety and frequency of aggressive interactions.
... Some behaviors, such a play-biting, were recorded for the
first time in the new enclosure. Both gorillas were prone to regurgitation
and re-ingestion in their former cages. However, in the naturalistic
environments these abnormal behaviors were never observed."
Marriott BM, Marriott RW, Norris J,
Lee D 1993. A
semi-natural habitat for housing small, nonhuman primates.
Journal of Medical Primatology 22, 348-354
A semi-natural habitat was designed to house a group of squirrel
monkeys. Animals maintained in this environment were "healthy,
and none of the animals exhibited locomotor stereotypies."
McGuffey LH, McCully CL, Bernacky BJ, Blaney SM 2002. Incorporation
of an enrichment program into a study protocol involving long-term
restraint in macaques. Lab Animal 31(10), 37-39
"In our experience, the provision of periodic intervals
of unrestricted activity directly correlated with an increased
tolerance during relatively more extended periods of [chair] restraint."
O'Neill PL 1989. Short-term and long-term
benefits of environmental enrichment on laboratory rhesus monkeys
(Macaca mulatta) . American Zoo and Aquarium Association
(AZA) Regional Conference Proceedings, 616-625
The animals were transferred from their barren group cage to
a more spacious playroom equipped with climbing /perching structures
and swings for one hour per day, five days a week: The animals
showed a decline in the frequency of three [out of four] behavioral
disorders in the playpen. This therapeutic effect was nullified
back in the barren homecage."
*Pines MK, Kaplan
G, Rogers LJ 2007. A note on indoor and outdoor housing preferences
of common marmosets (Callithrix jacchus). Applied Animal Behaviour
Science 108(3-4), 348-353
"When given free access to move between their home cage
and outdoors, the marmosets spent 70% of their day in the outdoor
cage."
Seier JV, Loza J, Benjamin L 2004.
Housing and stereotyped behaviour: Some observations from an indoor
colony of vervet monkeys (Chlorocebus aethiops). Folia
Primatologica 75(Supplement 1), 332
Adult females displaying stereotypies in single cages were exposed
sequentially to a foraging log and an exercise cage, as well as
cages of varying complexity and dimensions. The animals “spent
most time in stereotypies when in unenriched single cages. This
was significantly reduced by the provision of either an exercise
cage or a foraging log. No stereotyped behaviour was observed
in the largest most enriched cages.“
Storey PL, Turner PV, Tremblay JL
2000. Environmental enrichment for rhesus macaques: A cost-effective
exercise cage. Contemporary Topics in Laboratory Animal Science
39(1), 14-16
"Increased visual attentiveness by other animals, decreased
self-directed biting and hair picking, and improved food consumption
was observed when rhesus macaques were permitted access to an
exercise cage for several hours daily."
Tustin GW, Williams LE, Brady AG 1996.
Rotational use of a recreational cage for
the environmental enrichment of Japanese macaques (Macaca fuscata). Laboratory Primate Newsletter 35(1),
5-7
The rotational use of a "recreation cage" resulted
in increased use of enrichment devices and a decrease in stereotypical
behaviors.
Wilkes MN, Lynch CS, Fontenot MB 2006. Outdoor housing decreases
self-injurious and stereotypic behavior in adult male rhesus macaques
( Macaca mulatta). American Journal of Primatology
68(Supplement ), 106 (Abstract)
Access to an outdoor area decreased self-injurious and stereotypical
behaviors in adult male rhesus who had been single-caged or group-housed
indoors.
Baker KC 1997. Straw and forage material
ameliorate abnormal behaviors in adult chimpanzees. Zoo Biology
16, 225-236
"In an [successful] effort to reduce abnormal behaviors,
especially regurgitation and reingestion, and promote higher activity
levels [locomoting and playing], straw and scattered forage material
were added to the enclosures of 13 indoor-housed chimpanzees living
in pairs and trios."
Baker KC, Springer DA 2006. Frequency
of feeding enrichment and response of laboratory nonhuman primates
to unfamiliar people. Journal of the American Association for
Laboratory Animal Science [Contemporary Topics in Laboratory Animal
Science] 45(1), 69-73
"The data presented support the hypothesis that levels
of treat feeding influence monkeys' receptivity to unfamiliar
people."
Bayne K, Dexter SL, Mainzer H, McCully
C, Campbell G, Yamada F 1992. The use of artificial turf as a foraging substrate
for individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1, 39-53
"An increasing trend in time spent foraging with a concomitant
decline in aberrant behaviour over a time period of six months
was particularly noteworthy [in the single-housed subjects]."
Bayne K, Dexter S, Suomi S 1992. A
preliminary survey of the incidence of abnormal behavior in rhesus
monkeys (Macaca mulatta) relative to housing condition.
Lab Animal 21(5), 38-46
"The greatest frequency of overall abnormal behavior and
stereotypic exploratory behavior was in the SC [single cage] condition,
and the lowest frequency of occurrence in the CC [corn crib] condition
... in IO [indoor/outdoor] runs, the animals showed no self-directed
behavior."
Bayne K, Mainzer H, Dexter SL, Campbell
G, Yamada F, Suomi SJ 1991. The reduction of abnormal behaviors
in individually housed rhesus monkeys (Macaca mulatta) with
a foraging/grooming board. American Journal of Primatology
23, 23-35
All of the single-housed "animals foraged from the board
to the point that a significant reduction in the level of abnormal
behavior was noted."
Bennett BT, Spector MR 1989. The use
of naturally occurring manipulanda to improve the psychological
well-being of singly housed baboons. Journal of the American
Veterinary Medical Association 194, 1782
The single-housed animals demonstrated a marked reduction of
stereotypy when they had corn-on-the-cob.
Bloomsmith MA, Alford PL, Maple TL
1988. Successful feeding enrichment for captive chimpanzees. American
Journal of Primatology 16, 155-164
Four feeding techniques were simultaneously implemented. "Agonistic,
abnormal, and grooming behaviors were significantly reduced."
Boccia ML 1989. Long-term
effects of a natural foraging task on aggression and stereotypies
in socially housed pigtail macaques. Laboratory Primate
Newsletter 28(2), 18-19
"Two months following the introduction of the foraging
task stereotypies remained depressed, and hairpulling remained
rare. In addition, bedding exploration and other types of exploration
remained elevated, and agonistic behaviors remained low."
Boccia ML, Hijazi AS 1998. A
foraging task reduces agonistic and stereotypic behaviors in pigtail
macaque social groups. Laboratory Primate Newsletter
37(3), 1-5
"The monkeys increased the time they spent engaged in
environmentally directed [foraging] behaviors, and this correlated
with a decrease in time spent in agonistic (for one group) and
abnormal behaviors (for both groups). ... Both groups also evidenced
declines in hairpulling. ... Stereotypies (such as pacing) also
significantly decreased in both groups."
Boinski S, Gross TS, Davis JK 1999.
Terrestrial predator alarm vocalizations are a valid monitor of
stress in captive brown capuchins (Cebus apella). Zoo
Biology 18, 295-312
"Our results are consistent with the interpretation that
in conditions of low environmental enrichment the study subjects
were more stressed, and therefore more reactive to the presence
of a threatening terrestrial stimulus (human observer), than when
in more enriched conditions."
Brent L, Eichberg JW 1991. Woodchip
bedding as enrichment for captive chimpanzees. American Journal
of Primatology 24, 91-92
"Abnormal behavior and environmental manipulation were
significantly lower during the woodchip [not mixed with food]
condition."
Brent L, Long KE 1995. The behavioral
response of individually caged baboons to feeding enrichment and
the standard diet: A preliminary report. Contemporary Topics
in Lab Animal Science 34(2), 65-69
"Increasing foraging opportunities in this study reduced
abnormal behaviors from 16.4% of the data points in the baseline
condition to 4.9% and 5.7% in the chow [normal feeding condition]
and feeder condition, respectively."
Brent L, Belik M 1997. The response
of group-housed baboons to three enrichment toys. Laboratory
Animals 31, 81-85
"Abnormal, cage-directed, inactive and self-directed behaviours
all significantly decreased after the [simultaneous] provision
of the toys."
Brown DL, Gold KC 1997. Effects of
straw bedding on non-social and abnormal behavior of captive lowland
gorillas (Gorilla gorilla gorilla). In Proceedings on
the 2nd International Conference on Environmental Enrichment
Holst B (ed), 27-35. Copenhagen Zoo, Frederiksberg
"Two individuals were frequently observed to hold their
ears or head while the exhibit was in an unbedded condition. This
behavior virtually disappeared in the enriched condition. ...
Of the eight individuals found to engage in coprophagy, five individuals
were observed to exhibit this behavior in solely the unbedded
condition." Individuals who engaged in regurgitation-reingestion
demonstrated lower levels of this behavior in the bedded condition.
Chamove AS, Anderson JR, Nash VJ 1984.
Social and environmental influences on self-aggression in monkeys.
Primates 25, 319-325
"It is clear that enriched environmental conditions reduced
SA [self-aggression]. Allowing monkeys to forage through clean
woodchips, even when there is no obvious incentive, substantially
reduced the level of this abnormal behavior."
Crockett CM, Bellanca RU, Heffernan
KS, Ronan DA, Bonn WF 2001. Puzzle
Ball foraging device for laboratory monkeys. Laboratory
Primate Newsletter 40(1), 4-7
"We were please that the empty Puzzle Balls were associated
with a reduction [approximately 60%] in abnormal behavior."
Eaton GG, Kelley ST, Iliff-Sizemore
SA 1993. Rawhide 'chew-bones' reduce abnormal behavior in individually
housed adult rhesus macaques. American Journal of Primatology
30, 308
"Self-clasp showed a significant decline when the rawhide
bones were present. We conclude that rawhide chew-bones are an
effective, and relatively inexpensive method of enriching the
environment of individually housed rhesus macaques."
Honess PE, Marin CM 2006. Enrichment
and aggression in primates. Neuroscience and Biobehavioral
Reviews 30, 413-346
"There is considerable evidence that primates housed under
impoverished conditions develop behavioural abnormalities, including,
in the most extreme example, self-harming behaviour. This has
implications for all contexts in which primates are maintained
in captivity from laboratories to zoos since by compromising the
animals' psychological well-being and allowing them to develop
behavioural abnormalities their value as appropriate educational
and research models is diminished. This review examines the extensive
body of literature documenting attempts to improve living conditions
with a view to correcting behavioural abnormalities and housing
primates in such a way that they are encouraged to exhibit a more
natural range and proportion of behaviours, including less self-directed
and social aggression. The results of housing, feeding, physical,
sensory and social enrichment efforts are examined with specific
focus on their effect on aggressive behaviour and variation in
their use and efficacy. It is concluded that while inappropriate
or poorly distributed enrichment may encourage aggressive competition,
enrichment that is species, sex, age and background appropriate
can dramatically reduce aggression, can eliminate abnormal behaviour
and substantially improve the welfare of primates maintained in
captivity."
Kessel AL, Brent L 1998. Cage toys
reduce abnormal behavior in individually housed pigtail macaques.
Journal of Applied Animal Welfare Science 1, 227-234
"Providing multiple manipulable toys as enrichment for
[single-caged] pigtail macaques was effective in reducing abnormal
behavior" during 30- min observation session.
Lam K, Rupniak NMJ, Iversen SD 1991.
Use
of a grooming and foraging substrate to reduce cage stereotypies
in macaques. Journal of Medical Primatology 20, 104-109
"Stereotyped behaviours were reduced by up to 73% by use
of the fleece pad both alone and with foraging crumbles."
Maki S, Alford PL, Bloomsmith MA,
Franklin J 1989. Food puzzle device simulating termite fishing
for captive chimpanzees (Pan troglodytes). American
Journal of Primatology 19(Supplement 1), 71-78
"Significant reductions of abnormal behavior and significant
increases in activity occurred with the pipe feeder's availability."
Meunier LD, Dukting JT, Landi MS 1989.
Modification of stereotypic behavior in rhesus monkeys using videotapes,
puzzlefeeders, and foraging boxes. Laboratory Animal Science
39, 479
"Results of this study demonstrate that foraging boxes
and puzzle feeders can reduce stereotypic behavior significantly
[in single-housed subjects]."
Murphy DE 1976. Enrichment
and occupational devices for orang utans and chimpanzees.
International Zoo News 137(23.5), 24-26
Subjects were provided with an artificial termite mount. "The
most encouraging result was a reduction in the female's stereotyped
pacing. The environmental enrichment of the chimp exhibit has
resulted in a decrease in observable coprophagy, a diversification
of the activities, and a probable improvement in the physical
and psychological condition of the animals."
Nadler RD, Herndon JG, Metz B, Ferrer
AC, Erwin J 1992. Environmental enrichment by varied feeding strategies
for individually caged young chimpanzees. In Chimpanzee Conservation
and Public Health: Environments for the Future Erwin J, Landon
JC (eds), 137-145. Diagnon/Bioqual, Rockville
"Providing an ear of unhusked corn on alternate days,
in addition to laboratory chow, resulted in more time spent contacting
food [primarily the corn] an hour after feeding than feeding laboratory
chow alone. Seven of eight [single-housed] animals exhibited less
stereotypy on the days they received the ear of corn. Stereotypical
behavior, which occurs at relatively low frequencies under natural
conditions, was reduced somewhat when the animals were fed three
[rather than one] meals."
Neu K, Lambeth S, Toback E, Schapiro
S 2001. Hay
can be used to decrease feces smearing in groups of captive chimpanzees.
American Journal of Primatology 54(Supplement 1), 78
Feces smearing on the walls decreased significantly when hay
was present compared to when no hay was available.
Poffe A, Melotto S, Gerrard PA 1995.
Comparison of four environmental enrichment strategies in captive
common marmosets (Callithrix jacchus). Primate Report
42, 24-25
"Access to the puzzles was accompanied by increase in
social interaction and activity and decrease in stereotypic behaviour.
This behavioural profile was also observed, to a lesser extent,
in animals exposed to the 'gum tree'. ... Novel objects alone
[toys] failed to significantly alter behaviour."
Preilowski B, Reger M, Engele H 1988.
Combining scientific experimentation with conventional housing:
A pilot study with rhesus monkeys. American Journal of Primatology
14, 223-234
Manipulatory activity required by the apparatus reduced motor
stereotypies but not self-biting in single-housed subjects.
Pyle DA, Bennett AL, Zarcone TJ, Turkkan.
J. S., Adams RJ, Hienz RD 1996. Use
of two food foraging devices by singly housed baboons. Laboratory
Primate Newsletter 35(2), 10-15
"Stereotypical behaviors are reduced [in single-housed
subjects] when the devices are present. In addition, the foraging
devices elicited species-typical behaviors such as foraging and
grooming, even after food appeared to be absent from the devices."
Roberts RL, Roytburd LA, Newman JD
1999. Puzzle feeders and gum feeders as environmental enrichment
for common marmosets. Contemporary Topics in Laboratory Animal
Science 38(5), 27-31
"Gum feeders and Puzzle-Feeders loaded with waxmoth larvae
are useful for reducing the rates of pacing and inactivity"
in single-housed and in pair-housed marmosets.
Steen Z 1995. Effects
of enriched food acquisition on activity budgets of two tamarin
species at Adelaide Zoo. International Zoo News 42,
284-298
Simple bamboo pipe feeder is described and tested in group-housed
animals. "The aim of the study was to [successfully] increase
foraging time with an increasing number of feeding devices [brawn
bowl, bamboo pipe]. ... Prior to the study large amounts of fur
were found in the nesting box of the golden tamarins. The zoo
vet suspected that this was a result of overgrooming. During and
after the study the overgrooming apparently ceased because the
animals had something else to do."
Taylor TD 2002. Feeding
enrichment for red-handed tamarins. The Shape of Enrichment
11(2), 1-3
Access to a 'feeding basket' [stuffed with straw mixed with
their normal feed and hung from a perch] and suspended sticks
smeared with acacia gum increased feeding activities while reducing
the incidence of stereotypy [primarily somersaulting], hyperactivity,
coprophagy and excessive grooming and scent marking in a 3-adult-member
group.
Watson L 1992. Effect
of an enrichment device on stereotypic and self-aggressive behaviors
in singly-caged macaques: A pilot study. Laboratory Primate
Newsletter 31(3), 8-10
"A [temporary] reduction in some behavior pathology was
noted, possibly due to replacing the stereotypic behaviors with
activities directed toward the feeder."
Weld K, Erwin J 1990. Provision of
manipulable objects to cynomolgus macaques promotes species-typical
behavior. American Journal of Primatology 20, 243
"A different pet toy was provided to each [single-caged]
monkey" during six weeks. "Self-directed abnormal behavior
was reduced or eliminated in all subjects in the presence of objects
but increased after removal of the toys."
Wiard J 1992. Reduction of regurgitation
and reingestion (R&R) in lowland gorillas at the Oklahoma
City Zoo. Gorilla Gazette 6(3), 6-7
"The addition of browse or hay to the diet of captive
gorilla reduces the occurrence of R&R [regurgitation-reingestion].
Novelty items tend to reduce R&R [only] for short periods
of time."
Brent L, Weaver D 1996. The
physiological and behavioral effects of radio music on singly
housed baboons. Journal of Medical Primatology 25,
370-374
Vocalization [of the single-housed subjects] was twice as high
when the radio was off. Blood pressure did not vary with radio
condition, but the heart rate was significantly lower when the
radio was playing.
Howell S, Roeder E, Nelson C, Fritz
J, Schwandt M 2002. The effect of music on the behavior of captive
chimpanzees (Pan troglodytes).
American Journal of Primatology 57, 83-84
"Results suggest music has a significant effect on behavior
of captive chimpanzees. It resulted in decreased aggression and
active exploratory behavior and increased inactive resting and
social behavior (principally social grooming). .. We suggest music
may have a calming effect on behavior and good potential as therapeutic
environmental enrichment."
*McDermott J,
Hauser MD 2007. Nonhuman primates prefer slow tempos but dislike
music overall. Cognition 104, 654-668
Both tamarins and marmosets preferred slow tempo to fast temp
music, and when allowed to choose between slow tempo musical stimuli
and silence they preferred silence.
Videan EN, Fritz F, Howell H, Murphy J 2007. Effects of two types
and two genre of music on social behavior in captive chimpanzees
(Pan troglodytes). Journal of the American Association for
Laboratory Animal Science [Contemporary Topics in Laboratory Animal
Science] 46(1)
"The purpose of this study was to test the effects of
2 different types (vocal versus instrumental) and 2 genres (classical
vocal versus 'easy-listening' vocal) of music on social behavior
in 31 female and 26 male chimpanzees (Pan troglodytes). Results
indicated that instrumental music was more effective at increasing
affiliative behavior in both male and female chimpanzees, whereas
vocal music was more effective at decreasing agonistic behavior.
A comparison of 2 genre of vocal music indicated that easy-listening
(slower tempo) vocal music was more effective at decreasing agonistic
behavior in male chimpanzees than classical (faster tempo) vocal
music. Agonistic behavior in females remained low (<0.5%) throughout
the study and was unaffected by music. These results indicate
that, like humans, captive chimpanzees react differently to various
types and genres of music. The reactions varied depending on both
the sex of the subject and the type of social behavior examined.
"
Wells DL, Coleman D, Challis MG 2006. A note on the effect
of auditory stimulation on the behaviour and welfare of zoo-housed
gorillas. Applied Animal Behaviour Science 100(3-4), 327-332
Six gorillas housed in Belfast Zoo "were exposed to three
conditions of auditory stimulation: a control (no auditory stimulation),
an ecologically relevant condition (rainforest sounds) and an
ecologically non-relevant condition (classical music). The gorillas'
behaviour was recorded in each condition using a scan-sampling
technique. There was no significant effect of the auditory environment
on the gorillas' behaviour, although animals tended to show more
behaviours suggestive of relaxation (i.e. resting, sitting) and
fewer behaviours typically associated with stress (i.e. aggression,
abnormal behaviour) during the ecologically relevant, and, in
particular, the non-relevant, conditions than the control. Overall,
findings suggest that certain types of auditory stimulation may
hold some merit as a method of enrichment for zoo-housed gorillas."
Alexander S, Fontenot MB 2003. Isosexual
social group formation for environmental enrichment in adult male
Macaca mulatta. AALAS [American Association for Laboratory
Animal Science] 54th National Meeting Official Program, 141
Isosexual groups [averag group size: 4.2 animals] of 80, previously
single-caged 4-10 years old male rhesus macaques were formed [group
formation protocol is not outlined]. "Thirty-one [38.8%]
of these animal had at least one prior incidence of SIB [self-injurious
biting]. .. During the year prior to group formation, the clinical
history of the subjects included a 20% of diarrhea, 1.0% incidence
of wound infection and 12.5% incidence of severeSIB requiring
pharmacological intervention and wound care. Animals with severe
SIB were treated pharmacologically for 2-11 months prior to group
formation. All of these cases were removed from treatment prior
to group formation. Over the 4-month period post formations <5.0%
of the animals were removed for treatment of minor fight wounds.
Less than 2.0% of the animals were removed for clinical purposed
(e.g., diarrhea, dehydration). No occurrence of sever SIB was
noted. We concluded that the formation of isosexual social groups
is a suitable alternative to individual housing of adult male
rhesus monkeys and may decrease the occurrence of SIB in a susceptibe
population."
Baker KC 1996. Chimpanzees in single
cages and small social groups: Effects of housing on behavior.
Contemporary Topics in Laboratory Animal Science 35(3),
71-74
Chimpanzees housed in pairs or trios showed fewer signs of
tension, anxiety and aggressiveness than those housed singly.
Baker KC 1997. Human interaction as
enrichment for captive chimpanzees: A preliminary report. American
Journal of Primatology 42, 92
"These results suggest that simple, unstructured affiliation
between humans and chimpanzees has a powerful impact on well-being,
promoting activity and relaxed conspecific interactions and ameliorating
undesirable behaviors [e.g., abnormal behaviors]."
Bayne K, Dexter SL, Suomi SJ 1991.
Social housing ameliorates behavioral pathology
in Cebus apella. Laboratory
Primate Newsletter 30(2), 9-12
Change from single- to group-housing "effectively reduced
stereotypic behaviors; however, it also was associated with more
passive behaviors being exhibited by the subjects. The concurrent
shifts in these components of the behavioral repertoire suggests
that the animals were in a calmer state when housed socially."
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).
Contemporary Topics in Laboratory Animal Science 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."
Bloomsmith MA, Baker KC, Ross SK,
Lambeth SP 1998. Enlarging chimpanzee social groups: The behavioral
course of introductions. American Journal of Primatology
45, 171
Stereotyped rocking declined in newly integrated individuals.
Boccia ML, Reite M, Laudenslager ML
1989. On the physiology of grooming in a pigtail macaque. Physiology
and Behavior 45, 667-670
When the subject received grooming from others, heart rate
was significantly lower than during self grooming, as well as
during other behaviors.
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. "Analysis of baseline behaviour verified substantial
durations of abnormal behaviour [9.8/30- min observations (33%
of time)]. We tested the effectiveness of ... positive reinforcement
training (PRT), food enrichment [fruits, frozen fruit/juice, foraging
devices], non-food enrichment [toys], and social enrichment (pair/trio).
...The social enrichment condition resulted in the most positive
behavioural changes, including ... near elimination of abnormal
behaviours [0.7/30-min observation (2% of time)]. Significant
reduction in total abnormal behaviour levels were also found for
other types of enrichment, but only social enrichment and PRT
were effective in reducing whole-body stereotypies. ... Animate
enrichment (human or conspecific stimulation), as opposed to inanimate
enrichment, provides optimal means of behaviour modification for
singly caged baboons."
Bushong D, Schapiro SJ, Bloomsmith
MA 1992. Self-aggression in nonhuman primates: A review of its
development/possible causes, methods of therapeutic treatment,
and its relevance to the zoo situation. American Zoo and Aquarium
Association (AZA) Regional Conference Proceedings, 723-728
"Social enrichment appears to be the most effective method
of reducing the development or frequency of abnormal behaviors."
... After the animals "were moved from single- to pair-housing,
preliminary analyses of individual behavior indicated that there
was a decrease in time spent in self-aggressive behaviors."
Choi GC 1993. Humans enrich the lives
of lab baboons. WARDS (Working for Animals Used in Research,
Drugs and Surgery) Newsletter 4, 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.
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
"The presence of a social partner reduced signs of behavioral
disturbance."
Coelho AM, Carey KD, Shade RE 1991.
Assessing the effects of social environment on blood pressure
and heart rates of baboon. American Journal of Primatology
23, 257-267
In the social companion condition, a subject was able to have
visual, tactile, and auditory interactions with his companion
through the wire mesh walls of the specially designed cages. "When
animals were housed with social companions their blood pressures
were consistently lower than when they were either housed individually
or with social strangers. ... Measurements of cardiovascular physiology
obtained under social housing may more closely model normal physiology
than ... individual housing."
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 show strong preference to spend time in close
proximity; 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."
Fritz P, Fritz J 1979. Resocialization
of chimpanzees. Journal of Medical Primatology 8, 202-221
"With the exception of Tim, stereotyped behaviors in other
individuals decreased almost immediately upon introduction of
a compatible cage mate and continued to decrease as socialization
proceeded."
Gonzalez CA, Coe CL, Levine S 1982.
Cortisol responses under different housing conditions in female
squirrel monkeys. Psychoneuroendocrinology 7, 209-216
Plasma levels of cortisol "were significantly lower in
pair-housed females than in those living in a social group or
individually. The increment in cortisol levels after stress (handling
and ether anesthesia) also was smaller in females housed in pairs."
Dominant and subordinate partners of female pairs did not differ
in their plasma cortisol levels.
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
A training protocol is briefly described which allows the keepers
through vocal and visual cues to herd the animals to a holding
area. Training sessions were "deterring stereotypic and abnormal
behaviour - such as excessive grooming and fur-pulling."
Goosen C 1988. Studies of disturbed
behaviour in macaques. In Biomedical Research in Primates.
Proceedings of the TNO Symposium Jonker M (ed), 67-74
Stereotyped locomotion amounted to about 20% of the time when
the subjects were housed solitary. The amount of time spent in
this behaviour was reduced to about 4% when the subjects had one
or more social partners.
*Gunnar MR, Gonzalez
CA, Levine S 1980. The role of peers in modifying behavioral distress
and pituitary-adrenal response to a novel environment in year-old
rhesus monkeys. Physiology and Behavior 25, 795-798
Infant rhesus macaques were captured from their social group
and placed in an unfamiliar environment for 24 hours either (a)
alone or (b) with another infant from the same group. When tested
alone, the animals exhibited significantly more signs of distress
- agitation, distress vocalization - than when they were tested
with a companion, indicating that the companion had a stress-buffering
effect.
Gust DA, Gordon TP, Brodie AR, McClure
HM 1994. Effect of a preferred companion in modulating stress
in adult female rhesus monkeys. Physiology and Behavior
55, 681-684
"Adult female rhesus monkeys exhibited a profound stress
response when removed from their social group to a novel environment.
Recovery time [of T cell subsets] was significantly enhanced by
the presence of a preferred companion."
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 formation protocol in a pole-and-collar housing system
is described. "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."
Hartner MK, Hall J, Penderghest J,
White E, Watson S, Clark L 2000. A novel approach to group-housing
male cynomolgus macaques in a pharmaceutical environment. Contemporary
Topics in Laboratory Animal Science 39(4), 67
"Twenty percent of our primates are maintained in a single-housed
environment. Of those single-housed animals, 40% exhibited moderate
to marked degrees of self-directed activity; i. e., hairpulling.
By contrast, none of the pair or group-housed animals exhibited
these behaviors. ... These primates are now more receptive to
handling and training, and will therefore be better animal models,
as noted by a marked decrease in vocalization and self-directed
behavior during pole/collar capture and chair restraint procedures."
*Hennessy MB
1984. Presence of companion moderates arousal of monkeys with
restricted social experience. Physiology and Behavior 33,
393-398
When placed in a novel environment for 30 minutes, juvenile
squirrel monkeys emitted significantly more high-pitched vocalizations
when tested alone than when tested in the presence of the companion.
A significant elevation of plasma cortisol was observed only when
animals were exposed to the novel environment alone.
Kessel AL, Brent L 1997. Rehabilitating
a rheboon (Macaca mulatta x Papio hamadryas cynocephalus),
from single housing to social housing: A case study. American
Journal of Primatology 42, 121
Abnormal behavior was reduced from 46% of observation time
in the single-housed condition to 4% after introduction to an
enclosure with ten other rhesus females.
Kessel A, Brent L 2001. The rehabilitation
of captive baboons. Journal of Medical Primatology 30,
71-80
"Eleven baboons who had been singly housed indoors for
an average of 5 years were moved to outdoor social groups in an
attempt to provide a more species-typical environment and reduce
high levels of abnormal behavior. ... Abnormal behavior decreased
significantly from an average of 14% of the observation time in
the single cages to 3% in the sixth month of social housing. Cage
manipulation and self-directed behaviors also significantly decreased."
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
"Self-abusive behaviors were recorded for five of the
ten subjects when singly housed, but were completely absent after
pair formation."
Lutz CK, Novak M 2005. Environmental
enrichment for nonhuman primates: Theory and application.
ILAR [Institute for Laboratory Animal Research] Journal
46(2), 178-191
"Only social contact satisfies the goal of promoting
a wide variety of species-typical activities while at the same
time reducing or preventing the development of abnormal behavior.
.. A number of toys should be provided initially and rotated on
a regular basis to maintain interest. .. At present, the most
effective form of enrichment for captive primates is social housing."
Mahoney CJ 1992. Some thoughts on
psychological enrichment. Lab Animal 21(5), 27,29,32-37
"Isolation 'wards' for ill animals and infectious study
chambers can have windows or transparent plastic panels between
cages, providing visual communication without interfering with
independent or filtered air-flow."
Mason WA 1960. Socially mediated reduction
in emotional responses of young rhesus monkeys. Journal of
Abnormal and Social Psychology 60, 100-110
"Previous observations that social stimuli may function
as a source of security and a means of mitigating emotional distress
in young primates are fully supported by the present results."
Miller LC, Bard KA, Juno CJ, Nadler
RD 1986. Behavioral responsiveness of young chimpanzees (Pan
troglodytes) to a novel environment. Folia Primatologica
47, 128-142
"Extreme distress reported previously for chimpanzees
and human children when tested alone in a novel situation was
rarely observed in these tests when an attachment figure [human
caretaker] was present."
*Minkel R 2007.
Pair-housing eliminates compulsive hair pulling: a case report.
Laboratory Animal Refinement and Enrichment Forum (electronic
discussion group) , September 27, 2007
http://groups.yahoo.com/group/LAREF/members
"At a previous institution we had a cyno 'Grandpa' who
suffered from severe hair pulling. He had removed practically
all hair from his body; all that was left was a patch in the middle
of his back that he could not reach! He was not shy about hiding
his idiosyncratic behavior at all and would contort into strange
positions to do it. The veterinarians tried various treatments
to alleviate the problem to no avail. We tried all the various
enrichment devices we could find; they would only keep him occupied
for a day or so. We pulled all the dividers from his cage to give
him more space; no luck. We were reluctant to pair him as he was
an older male who had been singly housed for so long, but there
was no other treatment option left.
We tried two unsuccessful pairings and finally settled on a newly
acquired juvenile male who was very rowdy and active (Grandpa
was quite the opposite: relaxed and sedate). The little guy, himself
was on his second pair attempt. During his first attempt all he
did was try to start a fight. To our great relief the new pair
worked out just fine. This truly "odd couple" got along
great from the start. Grandpa responded correctly, brought the
little guy in line, and actually perked up. The most surprising
part, however, was that Grandpa stopped hair pulling. He stopped
completely, and all his hair had grown back in the course of several
months.
Three years later Grandpa had not resumed his old habit, even
though his buddy had been removed for research-related reasons
one year after the original pair formation."
Missakian EA 1972. Effects of adult
social experience on patterns of reproductive activity of socially
deprived male rhesus monkeys (Macaca mulatta). Journal
of Personality and Social Psychology 21(1), 131-134
"The three [single-caged, socially deprived] male subjects
represented examples of severely disturbed animals as witnessed
by rates of stereotyped behavior (self-aggression, stereotyped
locomotion). The problem under investigation involved the extent
to which social group experience as an adult could modify and/or
reverse atypical behaviors produced by rearing under conditions
of social deprivation." Two males showed a decrease in both
stereotyped locomotion and self-aggression after being introduced
into a group of rhesus macaques.
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."
Reimers M, Schwarzenberger F, Preuschoft S 2007. Rehabilitation
of research chimpanzees: Stress and coping after long-term isolation.
Hormones and Behavior in print
"Permanent retirement from biomedical research in combination
with therapeutic resocialization maximizing chimpanzees' situation
control resulted in reduced fecal cortisol metabolite levels.
Our results indicate that chimpanzees can recover from severe
social deprivation, and may experience resocialization as less
stressful than solitary housing."
Roberts SJ, Platt ML 2004. Pair-housing
macaques with biomedical implants: a safe and practical alternative
to single-housing. American Journal of Primatology 62(Supplement),
96-97
”Recognition of the importance of social interaction for
primate well-being has led to new USDA guidelines recommending
that animal facilities provide social enrichment for captive primates,
as long as doing so does not endanger the animals or interfere
with research goals. Group- or pair-housing is the best way to
provide social enrichment, but many primates used in medical research
are housed singly because they have implants which may make them
more vulnerable to inflicted injury. In addition, pairing adult
male monkeys is often considered too difficult and too impractical
to attempt. The goal of this study was to evaluate these assumptions.
Eight adult male rhesus macaques (Macaca mulatta) and two adult
male crab-eating macaques (Macaca fascicularis) were evaluated
for pairing and then housed with a compatible partner for up to
three years. During the period of study, 9 of the 10 monkeys received
cranial and scleral search coil implants. On average, each monkey
was compatible with 69% of partners, and this high degree of compatibility
allowed monkeys to be paired continuously within three weeks of
initial evaluation. Moreover, the rate of implant failure during
pair-housing (0.07 failures per month) was not significantly different
from the rate of implant failure when monkeys were singly-housed
(0.098). These data demonstrate that pair-housing provides a safe
and practical social alternative to single-housing for adult male
macaques with biomedical implants.“
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
"Three adults exhibiting stereotypical behavior abandoned
their peculiar habits after they had lived with their young companions
for four months."
Reinhardt V, Houser WD, Eisele S,
Cowley D, Vertein R 1988. Behavior
responses of unrelated rhesus monkey females paired for the purpose
of environmental enrichment. American Journal of Primatology
14, 135-140
Six of seven animals abandoned behavioral disorders within
the first four weeks of living together with a companion.
Reinhardt V, Houser WD, Cowley D,
Eisele S, Vertein R 1989. Alternatives to single caging of rhesus monkeys
(Macaca mulatta ) used in research.
Zeitschrift für Versuchstierkunde [Journal of Experimental
Animal Science] 32, 275-279
"The present investigation also demonstrates that pairing
caged rhesus monkeys with compatible conspecifics does not interfere
with a number of common research protocols [e.g., headcap implantation,
experimental surgery, blood collection]. Our experiences even
suggest that distress related to handling or restraint is reduced
by the presence of the familiar companion."
Reinhardt V 1990. Social
enrichment for laboratory primates: A critical review. Laboratory
Primate Newsletter 29(3), 7-11
"23% (54/237) of individually caged, but only 10% (38/382)
of pair-housed rhesus monkeys required medical treatment."
Reinhardt V 1999. Pair-housing
overcomes self-biting behavior in macaques. Laboratory
Primate Newsletter 38(1), 4
Subjects exhibited self-biting behavior predictably in the
presence of personnel."The transfer to a compatible social-housing
arrangement [isosexual pair-housing] effectively cured the [seven]
rhesus subjects from the behavioral pathology of habitual self-biting."
Rukstalis M, French JA 2005. Vocal
buffering of the stress response: exposure to conspecific vocalizations
moderates urinary cortisol excretion in isolated marmosets. Hormones
and Behavior 47, 1-7
"For many species, the presence of a significant social
partner can lessen the behavioral and physiological responses
to stressful stimuli. This study examined whether a single, individually
specific, signature vocalization (phee call) could attenuate the
physiological stress response that is induced in marmosets by
housing them in short-term social isolation. .. Isolated marmosets
exposed to a familiar pair mate's vocalization showed significantly
lower levels of urinary cortisol than when exposed to unfamiliar
marmoset vocalizations (P <0.04) or to no auditory stimuli
(P <0.03). .. The results presented here provide the first
evidence that a single, individually specific communication signal
can decrease the magnitude of a physiological stress response
in a manner analogous to the physical presence of a social partner,
a process we term vocal buffering."
Ruppenthal GC, Walker CG, Sackett
GP 1991. Rearing infant monkeys (Macaca nemestrina) in
pairs produces deficient social development compared with rearing
in single cages. American Journal of Primatology 25, 103-113
In contrast to singly caged infants, pair-reared infants failed
to show "rock/huddle/self clasp and stereotypy categories."
Schapiro SJ, Bushong D 1994. Effects of enrichment on veterinary treatment
of laboratory rhesus macaques (Macaca mulatta). Animal Welfare 3, 25-36
"Diarrhea-related problems typical for singly-housed animals
and trauma-related problems typical of group-housed animals were
not as prominent in the pairs."
Schapiro SJ, Nehete PN, Perlman JE,
Sastry KJ 2000. A comparison of cell-mediated immune responses
in rhesus macaques housed singly, in pairs, or in groups . Applied
Animal Behaviour Science 68, 67-84
"The data demonstrate that social housing condition affects
immune responses. While not unidirectional, these effects generally
suggest enhanced immune responses for socially housed animals.
.... It is our contention that strong social relationships, particularly
the affiliative interactions that characterize our pair housed
monkeys, may diminish the likelihood of severe infection with
potentially diarrhea-inducing agents. ... Since rhesus monkeys
live socially in nature, and the immune responses of singly housed
animals differed from those housed socially, there is considerable
motivation and justification for suggesting that the use of singly
housed rhesus macaques may complicate interpretations of normal
immunological responses."
Schapiro SJ 2002. Effects of social
manipulations and environmental enrichment on behavior and cell-mediated
immune responses in rhesus macaques. Pharmacology, Biochemistry
and Behavior 73, 271-278
"In general, enrichment of the inanimate environment with
toys, structures, foraging devices, and/or videotapes increased
the amount of species-typical behavior expressed by the monkeys,
but did not affect their immune responses. Housing monkeys socially,
on the other hand, not only resulted in increased time spent in
species-typical activities, but also resulted in (1) decreases
in time spent in abnormal behavior and (2) changes in a number
of immune parameters."
Schnell CR, Gerber P 1997. Training
and remote monitoring of cardiovascular parameters in non-human
primates. Primate Report 49, 61-70
"Training of non-human primates to handling and experimental
procedure will reduce the variance and increase the significant
level of observed changes, allows the measurement of normal physiological
parameters and finally reduces the number of animals used in an
experiment."
Steinbacher EA, Setser JJ, Morris TD, Gumpf D 2006. Development
and implementation of a program for the social housing of nonhuman
primates on toxicology studies. AALAS [American Association
for Laboratory Animal Science] 57th National Meeting Official
Program , 157 (Abstract)
"We developed a step-wise procedure for social housing
animals (cynomolgus and rhesus) into pairs, triads or quads based
on the study design. Nonhuman primates that were socially housed
showed signs of better physical and psychological health, thereby
greatly reducing abnormal behaviors and stereotypies, such as
self-biting, that could potentially compromise study data. Based
on the success of our social housing program, all nonhuman primate
studies longer than 28 d will be socially housed unless otherwise
approved by our institutional ACUC.
Thompson MA, Bloomsmith MA, Taylor
LL 1991. A
canine companion for a nursery-reared infant chimpanzee. Laboratory
Primate Newsletter 30(2), 1-4
"Reduction in rocking and other stress-related behaviors
in the dog's presence is a strong argument for providing nursery-reared
chimpanzees with dog companions. We have safely housed dogs with
single infants as well as with small groups of infants, until
infants reach about three years of age."
Van Loo P, Skoumbourdis E, Reinhardt
V 2006. Postsurgical
pairing: a discussion by the Refinement & Enrichment Forum.
Animal Technology and Welfare 5, 17-19
"It is my experience with rhesus macaques that it is advisable
to pair an animal after surgery as soon as possible with his or
her compatible companion. We did this especially with animals
after one of them had head cap implant surgery. The animals recover
better from the surgery stress when their familiar companion is
with them than when they are alone."
Wait C, Buchanan-Smith H, Morris K
2002. The effects of caretaker-primate relationships on primates
in the laboratory. Journal of Applied Animal Welfare Science
5, 309-319
Group-housed "animals who had friendly relationships with
caretakers were less disturbed by routine husbandry procedures.
.. Caretakers are much more likely to sustain scratches or bites
from animals who are fearful and aggressive towardd them."
Weed JL, Wagner PO, Byrum R, Parrish
S, Knezevich M, Powell DA 2003. Treatment of persistent self-injurious
behavior in rhesus monkeys throuth socialization: A preliminary
report. Contemporary Topics in Laboratory Animal Science 42(5),
21-23
Six individually caged males who engaged in persistent self-injurious
behavior (SIB) were vasectomized and subsequently paired with
females. The incidence of SIB was "markedly reduced for all
male monkeys after social pairing." One male engaged in severe
SIB after 32 months of pair-housing when he was temporarily removed
from his partner for a procedure.
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."
Cary M, Valentine B, Hill W 2000.
The effect of mother-infant separation in captive baboons on time
intervals to first postpartum estrus, confirmed pregnancy and
subsequent parturition. AALAS [American Association for Laboratory
Animal Science] 51st National Meeting Official Program , 126-127
"It is generally thought that early forced-weaning of
infants would reduce the time from parturition to the first fertile
postpartum estrus thus maximizing reproductive efficiency. ...
From a survey of 23 animal records we determined the following
values for mothers of both forced and naturally weaned infants:
days to first postpartum cycle and days from first postpartum
cycle to confirmed pregnancy. Mothers of naturally-weaned animals
(those with infants) first cycled at 174 ± 31 days and
were confirmed pregnant 26 ± 13 days after this. Conversely,
mothers of force-weaned infants (weaning at 180 ± 16 days)
first cycled at 187 ± 8 days and were confirmed pregnant
55 ± 26 days later. From these observations we suggest
that both groups (mothers of force-weaned versus naturally-weaned
infants) require similar times to exhibit their first postpartum
estrus, but mothers of naturally-weaned infants appear to breed
back more quickly (approximately one cycle) than those of force-weaned
infants."
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
"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."
Mason WA 1991. Effects of social interaction
on well-being: Development aspects. Laboratory Animal Science
41, 323-328
"Captive animals will be served best if developing individuals
are raised at least through weaning by their biological mothers
and have the experience of living in a social group that approximates
the size and age-sex composition of the group in which they would
develop in nature. ... It seems unlikely, however, that peer experience
alone can provide a practical alternative to mother-rearing."
Valentine B, Cary M, Stanley J, White
G, Wallis J 1999. The timing of mother-infant separation and its
effect on postpartum estrus and subsequent conception in captive
baboons. American Journal of Primatology 49, 110
"There was no correlation between infant removal age and
duration until next conception. ... Postpartum cyclicity usually
resumed before infant removal. Subsequent conception, however,
was not significantly influenced by infant removal. This study
indicates that early forced weaning did not accomplish the goal
of increased reproductive output. These findings - in addition
to the concern for proper psychological development - suggest
the better strategy is to allow infants to be naturally weaned
by mothers."
Wallis J, Valentine B 2001. Early
vs. natural weaning in captive baboons: The effect on timing of
postpartum estrus and next conception. Laboratory Primate
Newsletter 40(1), 10-13
"We examined the details of 73 recorded pregnancies of
45 adult females. ... The results of this study indicate that
forced infant weaning did not improve reproductive productivity
in our colony of baboons. In fact, the data indicate that most
females resumed their reproductive cycles well before infant removal
and, when given the opportunity for natural weaning, the females
conceived while their previous infants were still dependent upon
them. .. The potential benefits of allowing infants to remain
with their mothers throughout childhood are obvious."
(7) Working with Cooperative Animals
Bentson KL, Capitanio JP, Mendoza
SP 2003. Cortisol responses to immobilization with Telazol or
ketamine in baboons (Papio cynocephalus/anubis) and rhesus macaques
(Macaca mulatta). Journal of Medical Primalogy 32, 148-160
"The injection and blood sampling process increased cortisol
levels in monkeys not trained to extend an arm but exerted no
effect on cortisol in trained macaques.”
Bloomsmith MA, Marr MJ, Maple TL 2007. Addressing nonhuman
primate behavioral problems through the application of operant
conditioning: Is the human treatment approach a useful model?
Applied Animal Welfare Science 102(3-4), 205-222
"Training by the systematic application of operant conditioning
has been widely applied in the care, management, exhibition, and
study of nonhuman primates and many other species, but is less
often used to control problematic animal behavior such as stereotyped
behavior or self-injurious behavior... Virtually all the techniques
found to be effective treatments of stereotypy and self-injurious
behavior in humans are directly applicable to similar behaviors
in captive nonhuman primates. Thus the human work can serve as
a model for how we can enhance our attempts to address behavioral
problems in captive nonhuman primates."
Cross N, Pines MK, Rogers LJ 2004.
Saliva sampling to assess cortisol levels in unrestrained common
marmosets and the effect of behavioral stress. American Journal
of Primatology 62, 107-114
"We report a method for taking saliva samples from unrestrained,
captive marmosets (Callithrix jacchus) to assess levels of free
cortisol. Saliva samples can be obtained reliably, without any
habituation, by encouraging the marmosets to lick and chew a cotton-wool
bud coated in banana. Saliva is thus left on the bud. We also
tested sweetened fruit-drink crystals and a number of other substances,
but none of these attracted all of the marmosets, and even flavors
that were effective once soon lost their attraction. .. A first
experiment showed that the marmosets exhibited a rise in salivary
cortisol levels in response to social isolation. A second experiment
showed elevation of cortisol during a period when the marmosets
were disturbed by increased human activity and noise levels in
the building in which they were housed. Hence, this method of
saliva sampling is a convenient, noninvasive means of assessing
cortisol levels in marmosets.“
Elvidge H, Challis JRG, Robinson JS,
Roper C, Thorburn GD 1976. Influence of handling and sedation
on plasma cortisol in rhesus monkeys (Macaca mulatta).
Journal of Endocrinology 70, 325-326
"The present study shows that it is possible by long-term
regular training to achieve mean cortisol values which are significantly
lower than in untrained or anaesthetized animals."
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."
Iliff SA, Friscino BH, Anderson LC
2004. Refinement of study design using positive reinforcement
training in macaques. Folia Primatologica 75(Supplement
1), 282-283
”Implementation of Positive Reinforcement Training (PRT)
to refine and modify study procedures conducted with rhesus macaques
results in enhanced welfare for both animals and caregivers. Capitalizing
on the macaques intelligence and their capability to learn and
perform tasks with appropriate motivation, PRT can reduce or eliminate
the need for sedatives or restraint. PRT is useful for standard
husbandry procedures such as feeding and transferring animals
between cages. It can also be used to facilitate sample collection
from animals. Standard pharmacokinetic or metabolism study paradigms
for evaluation of pharmaceutical test compounds require frequent
collection of blood, bile and/or other body fluids from animals
instrumented with catheters and subcutaneous access ports. Collection
of these samples can be technically challenging, time consuming
and potentially stressful for both personnel and the animals.
However, when PRT is used to conduct sampling procedures in the
animals home enclosure, stress is minimized as evidenced by lower
cortisol levels.”
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."
Lambeth SP, Hau J, Perlman JE, Martino
M, Schapiro SJ 2006. Positive reinforcement training affects hematologic
and serum chemistry values in captive chimpanzees (Pan troglodytes).
American Journal of Primatology 68, 245-256
"Positive reinforcement training (PRT) techniques have
received considerable attention for their stress reduction potential
in the behavioral management of captive nonhuman primates. However,
few published empirical studies have provided physiological data
to support this position. To address this issue, PRT techniques
were used to train chimpanzees (Pan troglodytes) to voluntarily
present a leg for an intramuscular (IM) injection of anesthetic.
Hematology and serum chemistry profiles were collected from healthy
chimpanzees (n=128) of both sexes and various ages during their
routine annual physical examinations over a 7-year period. Specific
variables potentially indicative of acute stress (i.e., total
white blood cell (WBC) counts, absolute segmented neutrophils
(SEG), glucose (GLU) levels, and hematocrit (HCT) levels) were
analyzed to determine whether the method used to administer the
anesthetic (voluntary present for injection vs. involuntary injection)
affected the physiological parameters. Subjects that voluntarily
presented for an anesthetic injection had significantly lower
mean total WBC counts, SEG, and GLU levels than subjects that
were involuntarily anesthetized by more traditional means."
Lambeth SP, Hau J, Perlman JE, Schapiro SJ 2006. Positive reinforcement
training and physiological responses in chimpanzees. AALAS
[American Association for Laboratory Animal Science] 57th National
Meeting Official Program , 160 (Abstract)
"A subset of variables potentially indicative of acute
stress were analyzed to determine if the method of adminstration
of anesthetic (voluntary present for injection compared with nonvoluntary
injection) and/or the method of obtaining the blood sample (voluntary
compared with anesthesized) affected these physiogical parameters.
Those subjects that voluntarily presented for an anesthetic injection
and/or venipuncture differed significantly on many of these parameters
from those subjects that were nonvonluntarily anesthetized by
more traditional means or whose blood was obtained following anesthesia.
This data set objectively demonstrates that positive reinforcement
training for behaviors relevant to the blood sampling process
significantly affects some of the physiological measures correlated
with stress responses in captive chimpanzees."
McKinley J, Buchanan-Smith HM, Morris
K 2002. Training common marmosets (Callithrix jacchus)
to co-operate during routine laboratory procedures: Reliability
and time investment. In XIXth Congress of the International
Primatological Society, Abstracts - Caring for Primates 183-184.
Mammalogical Society of China, Beijing, China
"Nine pairs of ... marmosets were target trained to allow
in-homecage weighing" and six pairs were trained to provide
urine samples on request. Behavioural data showed that "increased
positive interactions with humans as a consequence of training
reduced stress as indicated by significantly less scent-marking,
self-scratching and tsk and phee vocalisation. ... Data collection
with trained animals was significantly faster than using standard
techniques."
Michael RP, Setchell KDR, Plant TM
1974. Diurnal changes in plasma testosterone and studies on plasma
corticosteroids in non-anaesthetized male rhesus monkeys (Macaca
mulatta). Journal of Endocrinology 63, 325-335
Authors evaluated plasma corticosteroid concentrations in male
rhesus macaques who "were trained to enter voluntarily a
restraining apparatus" and permitted venipuncture without
showing signs of stress. Basal cortisol values were 30% lower
than previously reported for different, untrained animals.
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."
Reinhardt V 1992. Improved
handling of experimental rhesus monkeys. In The Inevitable
Bond. Examining Scientist-Animal Interactions Davis H, Balfour
AD (eds), 171-177. Cambridge University Press, Cambridge
The significant increase of serum cortisol concentration associated
with involuntary manual or mechanical restraint during venipuncture
was absent in females who were trained to voluntarily cooperate
during the procedure.
Schnell CR, Gerber P 1997. Training
and remote monitoring of cardiovascular parameters in non-human
primates. Primate Report 49, 61-70
"We could prove that marmosets can be trained to participate
willingly in cage restraint and to urine sampling by the use of
appropriate (banana milk-shake) rewards. Under this prospect,
they showed no behavioral and cardiovascular signs of distress."
The "training of non-human primates to handling and experimental
procedure will reduce the variance and increase the significant
level of observed changes, allows the measurement of normal physiological
parameters and finally reduces the number of animals used in an
experiment."
Smith CC, Ansevin A 1957. Blood pressure
of the normal rhesus monkey. Proceedings of the Society for
Experimental Biology and Medicine 96, 428-432
"Most [single-housed] monkeys could be trained to sit
quietly" during blood pressure measurements. "The procedure
used in handling the monkeys was an important factor in securing
reproducible blood pressure measurement."
Smith M, Barley J, Down N, Francis
R, Feurtado M, Kerwin A, Patterson-Kane E, Sherwin C, Reinhardt
V 2005. Catching
animals who have escaped from their primary enclosure: A discussion
by the Laboratory Animal Refinement & Enrichment Forum.
Animal Technology and Welfare 4(1), 41-44
"Capturing rodents, nonhuman primates and birds who
have escaped from their primary enclosure does not need to be
a chaotic event and does not necessitate the use of stress-inducing,
possibly injurious methods in most cases. The application of basic
ethological principles plus compassion can make a big difference,
turning the recapture procedure into a harmless event both for
the escapee and for the personnel."
Schwindaman D 1991. The 1985 animal
welfare act amendments. In Through the Looking Glass. Issues
of Psychological Well-being in Captive Nonhuman Primates Novak
MA, Petto AJ (eds), 26-32. American Psychological Association,
Washington DC
"To reduce the stress and pain of laboratory animals,
nontraumatic restraining techniques must be taught. ... We believe
that teaching of procedural skills is crucial for maintaining
high research standards within the laboratory."
Tiefenbacher S, Lee B, Meyer JS, Spealman
RD 2003. Noninvasive technique for the repeated sampling of salivary
free cortisol in awake, unrestrained squirrel monkeys. American
Journal of Primatology 60, 69-75
”Individually housed adult male squirrel monkeys were trained
to chew on dental rope attached to a pole, from which saliva was
extracted by centrifugation and analyzed for cortisol. .. Eight
of nine monkeys readily acquired the task, reliably providing
adequate saliva samples for the assay. .. The described sampling
technique provides a reliable and sensitive means for repeated
measurement of HPA activity in unrestrained, awake squirrel monkeys.“
Wall HS, Worthman C, Else JG 1985.
Effects of ketamine anaesthesia, stress and repeated bleeding
on the haematology of vervet monkeys. Laboratory Animals
19, 138-144
"10 adult [single-housed] non-pregnant females were trained
to present a limb for unstressed sampling."
(8) Treatment of Animals in their Home Enclosure
Nelms R, Davis BK, Tansey G, Raber
JM 2001. Utilization of training techniques to minimize distress
and facilitate the treatment of a chronically ill macaque. 2001
AALAS [American Association for Laboratory Animal Science] Official
Program, 97-98
"In order to permit the more frequent measurement of blood
glucose, at times up to eight measurements a day, with minimal
or no distress to the animals, we trained the monkey [long-tailed
macaque with unspecified gender] to voluntarily present the hand
[in the homecage] and accept a finger stick for the collection
of blood."
Reinhardt V, Cowley D, Scheffler J,
Vertein R, Wegner F 1990. Cortisol
response of female rhesus monkeys to venipuncture in homecage
versus venipuncture in restraint apparatus. Journal of
Medical Primatology 19, 601-606
All subjects were well habituated to blood collection, and
it was not necessary to immobilize them; they readily presented
a leg for venipuncture. In single monkeys venipunctured in the
restraint apparatus, cortisol concentrations were on average 50%
higher 15 minutes after venipuncture; this elevation was significant
(p<0.001). The magnitude of cortisol elevation was only 18%
in single monkeys venipunctured in the homecage; this elevation
was not significant (p>0.1).
Reinhardt V, Cowley D, Eisele S, Scheffler
J 1991. Avoiding
undue cortisol responses to venipuncture in adult male rhesus
macaques. Animal Technology 42, 83-86
Six adult rhesus males were: a) habituated to actively cooperate
during venipuncture away from the homecage in a treatment squeeze
cage, and b) trained to actively cooperate during venipuncture
in the homecage. The magnitude of cortisol increase was significant
when the males were venipunctured in the hallways but not when
they were venipunctured in the homecage. "It was concluded
that venipuncture per se was not a physiologically distressing
event. It became distressing only when it was associated with
a temporary removal from the homecage."
Reinhardt V, Cowley D 1992. In-homecage
blood collection from conscious stumptailed macaques. Animal
Welfare 1, 249-255
"After entering an animal room it took between 1.5 and
2 minutes to draw a blood sample from a successfully trained subject."
Blood collection of the pair-housed, trained animals was not accompanied
by an increase in serum cortisol concentration.
Thomsen R, Voigt CC 2006. Non-invasive
blood sampling from primates using laboratory-bred blood-sucking
bugs (Dipetalogaster maximus; Reduviidae, Heteroptera).
Primates in press
"Primates are easily stressed by the conventional veterinary
blood sampling routine and consequently, measured blood parameters
may be biased. In this study, we tested blood-sucking bugs (Dipetalogaster
maximus) on one lemur and two ape species (Microcebus murinus,
Pongo abelii, Pan paniscus) as an alternative, non-invasive technique
for bleeding primates. Within time periods of between 6 and 62
min we obtained blood volumes of 0.01-2.4 ml in 11 out of 12 trials
from all three species. Therefore, we conclude that these bugs
represent a new, gentle and effective tool for bleeding captive
primates without stress."
Reinhardt V 1997. Lighting
conditions for laboratory monkeys: Are they adequate? Animal
Welfare Information Center(AWIC) Newsletter 8(2), 3-6
"The prevailing monkey cage arrangement makes adequate,
that is uniform, illumination impossible, because the cages of
upper-rows block the light from entering the cages of lower-rows.
Caging all animals at the same level of the room is the only solution
to the problem of uneven lighting conditions."
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
"Lighting must be uniformly diffused throughout animal
facilities and provide sufficient illumination to aid in maintaining
good housekeeping practices, adequate cleaning, adequate inspection
of animals, and for the well-being of animals."