J American
Association for Laboratory Animal
Science
2006;
45(5):35-43
Effects
of Outdoor Housing on
Self-Injurious
and
Stereotypic Behavior
in Adult
Male Rhesus Macaques (Macaca
mulatta)
M Babette Fontenot, Mandi N Wilkes, and
Cheryl S Lynch
Psychology
Department
new iberia research center,
behavioral sciences University of louisiana at
lafayette,
Abstract: We examined the effects of
outdoor housing on self-injurious and
stereotypic behavior in adult male rhesus
macaques with a history of self-wounding that
were previously singly housed indoors for at
least 4 y prior to the study.
Baseline behavioral observations were
collected over 2.5 mo. In phase 1, animals were
relocated outdoors in 1 of 2 experimental
conditions, grouphoused (n =8) or single-housed
(n =5), for 6 wk. In phase 2, group-housed
animals were observed outdoors for an additional
6 wk.
Behavioral observations were done using
focal sampling techniques. In phase 1, rates of
self-biting and self-directed stereotypies and
time spent displaying idiosyncratic
self-directed stereotypies decreased
significantly when group- and single-housed
animals were housed outdoors. Rates of
yawning and scratching were significantly
decreased for group- and single-housed animals
and, for group-housed animals, self-grooming
decreased with outdoor housing.
In phase 2, rates of self-biting, time
engaging in idiosyncratic self-directed
stereotypies, and yawning remained
significantly lower during weeks 7 through 12
(outdoor housing) compared with those under
indoor housing. Rates of scratching and time
spent self-grooming decreased significantly
during the first 6 wk but then returned to
baseline levels.
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 regardless of whether animals are
socially or individually housed.
In rhesus macaques, prolonged individual
housing, particularly if initiated at an early
age, is implicated as a leading contributing
factor to the development of self-injurious
behavior (SIB). Therefore, several studies have
examined the effects of socially housing animals
that exhibit SIB. Mitchell13 attempted to pair
juvenile social isolates with adults, age-mates,
or infants in a playroom for 15-min intervals,
but he found that exposing juveniles to adults
or age-mates did not significantly reduce
SIB.
However, the exposure was probably too brief
to realistically evaluate any positive effects
of socialization on these animals.Bayne, Dexter,
and Suomi2 compared animals that were housed
individually indoors with those that were housed
in outdoor groups in either runs or corncribs
and found that animals housed socially in
corncribs exhibited significantly lower rates of
SIB than those among monkeys housed individually
indoors.
Reinhardt15 showed that in 7 rhesus monkeys
paired with samesex partners, rates of SIB
decreased immediately in 3 animals, whereas they
diminished gradually over a 2-mo period in the
remaining 4 animals. Finally, Weed and
colleagues21 paired vasectomized monkeys with
females and found that instances of SIB were
"markedly reduced" in the males.
Overall, these studies suggest that social
housing may have ameliorative effects on rates
of SIB. However, it is unclear whether housing
animals in an outdoor environment contributes to
the effects of group housing. Therefore, we
investigated whether housing animals outdoors
reduces rates of SIB and amount of time
displaying stereotypic behavior more than does
group-housing alone.
Discussion
In phase 1, we found that when housed
outdoors, regardless of social housing, animals
displayed significantly (P < 0.05) lower
rates of biting and self-directed stereotypic
behavior and spent significantly (P < 0.05)
less time displaying idiosyncratic self-directed
behavior. Group-housed animals spent less time
pacing. However we had no evidence that outdoor
housing had an effect on self-wounding. In phase
2, we found that rates of biting, percentage of
total time spent displaying idiosyncratic
self-directed stereotypies, stereotypic body
movement, and pacing decreased over 12 wk of
outdoor
housing. Again, we found no evidence that
self-wounding was decreased in group-housed
animals over the 12-wk period.
In phase 1, rates of yawning and scratching
and percentages of total time spent manipulating
toys and in neutral behavior decreased and the
amount of time spent resting increased when
animals were housed outdoors. For animals housed
in grooutdoors, the amounts of time spent pacing
and self-groomingdecreased whereas the
percentage of total time spent locomoting and
scanning increased.
In phase 2, group-housed animals spent more
time scanning, resting, and locomoting and less
time manipulating toys when housed outdoors
throughout the 12-wk period. Rates of yawning
outdoors remained lower than indoor levels.
However, percentages of total time spent
self-grooming and in neutral behaviors as well
as the rate of scratching returned to baseline
levels.
The absence of effects of housing on
self-wounding could be related to our relatively
small sample size combined with observations
that self-wounding occurs only rarely and
sporadically among animals that self-bite. Lutz
and colleagues11found that although 25% of the
362 monkeys they examined engaged in
self-biting, only 11% had a veterinarian record
of SIB. Although we found evidence that
stereotypic behaviors and self-biting were
decreased in the present study, further research
is required to determine the effects, if any, of
outdoor housing on self-wounding.
One possible explanation for the reduction
in self-biting and self-directed and other
stereotypic behavior is suggested from the
results of Novak,14 who found that SIB could be
elicited by exposure to stressful procedures
such as husbandry routines or veterinary
procedures. At our facility, outdoor housing
provides more space for animals to avoid
close contact with care staff, and husbandry
routines are less labor intensive. In addition,
veterinary procedures typically are not done
outdoors. Insofar as yawning, scratching (phase
1), self-grooming (phase 1), and self-directed
behavior reflect levels of anxiety,1,3,16,17,20
decrease in these behaviors suggests that
outdoor housing was less stressful during the
first 6 wk. Among group-housed animals in weeks
7 through 12 of phase 2, scratching and
self-grooming returned to baseline levels and
may reflect increased tension among or between
the social groups.
In our study, 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; these increases
could have contributed to changes in physical
activity. Although previous research found that
reductions in cage size to 20% of that specified
by US Department of Agriculture regulations led
to decreased locomotion, increasing cage area to
148% of the mandated size had no effect on
either abnormal or normal behaviors of pigtailed
macaques (M. nemestrina). Similarly, in
long-tailed (M. fascicularis) and rhesus
macaques, increasing cage size did not have an
effect on abnormal behavior or activity level.
It should be noted that all of these studies
compared cage size effects on behavior in an
indoor environment. We found that group-housed
animals, which received the largest increase in
cage area, had significant increases in
locomotionand scanning and decreased pacing,
whereas these behaviors did not change
significantly in single-housed animals. These
results may have been influenced by increased
cage space. A follow-up study examining outdoor
housing in cages equivalent in dimension to
indoor cages is required to adequately
differentiate the potential effects of changes
in cage area from outdoor housing on
behavior.
In addition to increased space, outdoor
housing exposes animalsto natural perceptual
stimuli such as sunlight, dusk-dawntransition,
natural sounds, and temperature variation.
Ourobservations were done during the winter
months (November through February) when
temperatures averaged 14.8 C (range, 0 to 27.8
C), whereas indoor temperatures were relatively
constant (range, 22.2 to 26.7 C). Macaques may
budget their activity in order to save energy
when environmental temperatures are relatively
low. Therefore relatively cold environmental
temperatures may promote increases in
energy-conserving activities such as resting,
scanning, and locomotion, and decreases in
activitie such as pacing. We found that
environmental temperature altered scanning in
single-housed animals during phase 1 and neutral
behaviors in group-housed animals in phase 2.
However, we found no evidence that temperature
affected SIB, stereotypic, and most of the
general behavior examined. Seasonal studies with
a larger sample size would be required to fully
examine the potential role of environmental
temperature.
The results of our study generally support
Bayne, Dexter, and Suomi, who found that animals
socially housed in corncribs exhibited less
abnormal behavior compared to animals housed
individually indoors. However, further studies
are needed to determine whether the frequency of
self-wounding would be decreased by a change
from indoor to outdoor housing. Overall, our
results suggest that self-biting and
self-directed stereotypic behavior in rhesus
macaques with a history of SIB is significantly
reduced by outdoor housing, regardless of
whether animals are socially or individually
housed, and that, when possible, such a change
in housing improves well-being. As an adjunct to
outdoor housing or when outdoor housing is not
possible, pharmacological treatment may be
necessary.