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Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta).

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American Journal of Primatology 69:584–590 (2007)
BRIEF REPORT
Early Predictors of Self-Biting in Socially-Housed Rhesus
Macaques (Macaca mulatta)
CORRINE K. LUTZ1, ERNIE B. DAVIS2, ANGELA M. RUGGIERO1,
1
AND STEPHEN J. SUOMI
1
Laboratory of Comparative Ethology, NIH Animal Center, NICHD,
National Institutes of Health, Poolesville, Maryland
2
Research Animal Management Branch, NICHD, National Institutes of Health
The development of self-biting behavior in captive monkeys is little
understood and poses a serious risk to their well-being. Although early
rearing conditions may influence the expression of this behavior, not all
animals reared under similar conditions self-bite. The purpose of this
study was to examine the effects of three rearing conditions on biting
behavior and to determine whether early infant behavior can predict
later self-biting. The subjects were 370 rhesus macaques born at the
National Institutes of Health (NIH) Animal Center between 1994 and
2004. They were reared under three conditions: mother-reared in social
groups (n 5 183), peer-reared in groups of four (n 5 84), and surrogatepeer-reared (n 5 103). Significantly more surrogate-peer-reared animals
self-bit compared to peer-only or mother-reared animals. There was no
sex difference in self-biting, but this result may have been affected by a
sex bias in the number of observations. The durations of behaviors
exhibited by the surrogate-peer-reared subjects were recorded in 5-min
sessions twice a week from 2 to 6 months of age while the animals were in
their home cages and play groups. In the play-group situation, surrogatepeer-reared subjects who later self-bit were found to be less social and
exhibited less social clinging than those that did not self-bite. Home-cage
behavior did not predict later self-biting, but it did change with
increasing age: surrogate clinging and self-mouthing decreased, while
environmental exploration increased. Our findings suggest that surrogate
rearing in combination with lower levels of social contact during play may
be risk factors for the later development of self-biting behavior. Am. J.
Primatol. 69:584–590, 2007.
Published 2007 Wiley-Liss, Inc.y
Key words: Macaca mulatta; rearing; self-biting; social behavior
Contract grant sponsor: Intramural Research Program of the NICHD, NIH.
Correspondence to: Corrine Lutz, Southwest National Primate Research Center, P.O. Box 760549,
San Antonio, TX 78245-0549. E-mail: clutz@sfbr.org
Received 22 March 2006; revised 1 June 2006; revision accepted 13 June 2006
DOI 10.1002/ajp.20370
Published online 10 January 2007 in Wiley InterScience (www.interscience.wiley.com).
y
This article is a U.S. government work and, as such, is in the public domain in the United States
of America.
Published 2007 Wiley-Liss, Inc.
Early Predictors of Self-Biting / 585
INTRODUCTION
The development of self-biting behavior in captive monkeys can pose a risk to
their overall well-being. In one survey approximately 25% of individually housed
rhesus monkeys exhibited self-biting behavior, and approximately 40% of those
animals had at least one record of self-inflicted wounding [Lutz et al., 2003]. It is
not yet known whether biters and wounders are two separate populations, or
whether biters eventually wound themselves.
Social separation at an early age due to total isolation [Harlow & Harlow,
1962], partial isolation [Mason & Sponholz, 1963], or early separation after
social rearing [Lutz et al., 2003] has been cited as a risk factor for the
development of self-injurious behavior in rhesus macaques. Nursery-reared
pigtailed macaques have also been shown to display more self-abusive behavior
than mother-reared subjects [Bellanca & Crockett, 2002]. Although a generally
preferred rearing method is to rear the infant with the mother in social groups
[Ruppenthal et al., 1974], this is not always possible due to experimental
protocol, maternal rejection, or illness. Surrogate-rearing with an artificial
surrogate and daily playtime with peers has been promoted as a good alternative
[Mason, 1991]. Another type of rearing paradigm–rearing in a peer-only
group with continuous peer contact–is typically less preferred, in part because
it has been reported to result in greater clinging, fear, and social withdrawal in
paired pigtailed macaque infants [Ruppenthal et al., 1991]. However, the
success of peer-rearing may depend on the number of animals in the group.
Infants reared in groups of four typically fare better than infants reared in pairs.
In one study, rhesus infants reared in groups of four showed lower levels of
clinging than those reared in pairs, and, unlike the pair-reared subjects, were
sexually adequate as adults [Chamove et al., 1973]. Infants reared in groups
of four also showed few differences in Bayley test scores in comparison to
mother-reared infants. Out of 15 categories, they differed only in two. They
showed lower levels of hostility and higher levels of fearfulness during testing
[Clarke & Snipes, 1998].
Even when they are reared under similar conditions, only a portion of infant
monkeys develop self-injurious behavior later in life. This may be due in part
to inherent differences in the animals’ temperament. Individual differences
in behavioral traits among rhesus monkeys appear to influence how an animal
will respond to environmental and social challenges [Suomi, 1991]. Perhaps a
temperamental predisposition combined with specific rearing practices influence
whether an animal self-bites in response to subsequent environmental challenges
or stressors.
Because procedures such as environmental enrichment have generally not
been successful in eliminating self-injurious behavior from an animal’s behavioral
repertoire [Novak et al., 1998], early prediction and prevention may be the key.
The purpose of this study was to examine the effects of three rearing conditions
(mother-reared, surrogate-reared, and peer-reared) on self-biting behavior, and
to determine whether early infant behavior can predict the later development of
self-biting.
MATERIALS AND METHODS
Subjects
The subjects were 370 Macaca mulatta born at the NIH Animal Center
between 1994 and 2004. They ranged in age from 1 to 12 years during the
Am. J. Primatol. DOI 10.1002/ajp
586 / Lutz et al.
observation period. The subjects were reared in one of three rearing conditions:
mother-reared, surrogate-reared, and peer-reared. The mother-reared infants
were housed in social groups consisting of approximately 12–14 adult animals and
their offspring (n 5 183). The surrogate-reared infants were housed from birth in
individual cages containing an artificial surrogate. Starting at 1–2 months of age,
they were placed in play groups of four same-age peers for 2 hr per day, 5 days per
week (n 5 103). The peer-reared infants were housed continuously in groups of
four same-age peers starting at 1–2 months of age. Peer-reared infants were also
provided with artificial surrogates from birth until the youngest infant in the
group reached 4 months of age (n 5 84).
At approximately 8–10 months of age, all infants born in a given year
were removed from their respective rearing situations and placed into one
large social group of approximately 40 same-age peers. These groups were
then split into smaller breeding groups consisting of approximately 12–14
animals as the subjects matured. The animals in the breeding groups consisted of
subjects from all three rearing conditions, and they were all treated in a similar
manner.
Procedures
The subjects were routinely observed for self-biting behavior two times per
year from 2001 to 2005. This consisted of approximately 5 min of observation
per subject, during which time episodes of self-biting were recorded. Each subject
was observed an average of 5.5 times (range: 1–10). Observations were evenly
distributed by rearing condition (F(2,364) 5 0.24, P40). However, due in part to
colony management practices in which more females than males were retained
for breeding purposes, females were observed more often than males (6.9 vs. 4.35
times; (F(1,364) 5 76.48, Po0.05). As a result, the mean age of females was
greater than that of males (4.4 vs. 3.6 years; (F(1,364) 5 10.46, Po0.01), but there
was no age difference by rearing condition (F(2,364) 5 2.23, P40.05) and there
was no significant sex-by-rearing interaction (F(2,364) 5 1.01, P40.05).
Self-biting episodes that occurred in between routine observations were also
recorded. An animal was considered to be a self-biter if it was observed to self-bite
at least one time during either the routine or the chance observations. Mockbiting of the hand or forearm as part of a threat display directed toward another
individual was not recorded as a self-biting event.
Behavioral data were also recorded in a subset (n 5 97) of the surrogatereared infants for 4 months between the ages of 2 and 6 months. Two 5-min
observation sessions were conducted per week on the surrogate-reared
infants while they were alone in their home cage, and two 5-min sessions
were conducted per week while they were in their play groups. The durations of
the following behaviors were recorded: environmental explore (any manual,
pedal, or oral examination or manipulation of the physical environment), play
(attempts to initiate play with a neighbor via ‘‘play face,’’ nonaggressive chasing,
tagging, swatting, bobbing, biting, pulling, lunging, or mouthing), self-mouthing
(sucking at any bodily appendage or own hair), and self-directed behaviors (firm
manual or pedal gripping of self, self-grooming, self-scratching, self-biting, or
chewing nails). Clinging to the surrogate was also recorded in the home cage, and
social contact (proximity within arm’s reach of another animal, groom, and
receive groom) and social cling (touching its ventral surface to the other animal
with at least one arm or leg wrapped around the other animal) were recorded in
the play cage.
Am. J. Primatol. DOI 10.1002/ajp
Early Predictors of Self-Biting / 587
Data Analyses
Chi-square tests were conducted to assess the association between biting
status (biter or nonbiter) and rearing condition (mother-, surrogate-, or peerreared), and between biting status and sex. A two-sample t-test was conducted to
compare the mean age of biting and nonbiting subjects.
Four monthly means (months 2–5) were calculated from the behavioral data
for the surrogate-reared infants. Because of the resulting non-normal distributions, a square-root transformation was conducted on all of the behavioral
durations in both the play cage and the home cage, with the exceptions of social
contact and environmental explore in the play cage, and environmental explore
in the home cage.
Repeated-measures analyses of variance (ANOVAs) were conducted on the
behavioral data collected from the surrogate-reared animals. The within-subjects
variable was age (months 2–5) and the between-subjects variable was biting
status (biter or nonbiter).
RESULTS
Sex, Rearing, and Age Effects
Self-biting was observed in both the larger juvenile groups and the smaller
adult breeding groups. Self-biters were predominantly surrogate-reared
(w2(2) 5 55.06, Po0.001; Table I), but there was no sex difference in biting
behavior (w2(1) 5 0.025, P40.05; Table II). Animals that were observed to selfbite were slightly older on average than nonbiters (biters: 4.7 years, nonbiters:
3.9 years; t(1) 5 1.84, Po0.10). None of the subjects had a record of self-injury.
Behavior (Surrogate-Reared Subjects)
Play cage
Durations of social contact and social cling in the play cage were lower in
animals that later self-bit (social contact: F(1, 95) 5 4.76, Po0.05 [Fig. 1]; social
cling: F(1, 95) 5 4.52, Po0.05 [Fig. 2]). There was no group difference in
the remaining behaviors (environmental explore: F(1, 95) 5 0.06, P40.05; play:
F(1, 95) 5 0.59, P40.05; self-mouthing: F(1, 95) 5 0.50, P40.05; self-directed:
F(1, 95) 5 0.125, P40.05).
TABLE I. Self-Biters Were Predominantly Surrogate-Reared
Non-biter
Self-biter
80
84
181
23
0
2
Surrogate-reared
Peer-reared
Mother-reared
TABLE II. Self-Biting Did Not Vary by Sex
Male
Female
Non-biter
Self-biter
185
160
13
12
Am. J. Primatol. DOI 10.1002/ajp
588 / Lutz et al.
mean seconds per 5-minute session
160
140
120
100
80
60
40
non-biter
biter
20
0
month 2
month 3
month 4
month 5
Fig. 1. Subjects with a record of self-biting were less social in the play cage than nonbiters.
mean seconds per 5-minute session
30
25
20
15
10
5
0
non-biter
biter
month 2
month 3
month 4
month 5
Fig. 2. Subjects with a record of self-biting exhibited less social cling in the play cage than nonbiters.
Play-cage behavior did not change with age (environmental explore: F(3,
285) 5 0.26, P40.05; play: F(3, 285) 5 1.23, P40.05; self-mouthing: F(3, 285) 5 1.47,
P40.05; self-directed: F(3, 285) 5 2.61, P40.05; social contact: F(3, 285) 5 0.69,
P40.05; social cling: F(3, 285) 5 0.66, P40.05).
Home cage
Home-cage behavior did not predict later self-biting in surrogate-reared
infants (environmental explore: F(1, 95) 5 0.41, P40.05; play: F(1, 95) 5 0.54,
P40.05; self-mouthing: F(1, 95) 5 0.275, P40.05; self-directed: F(1, 95) 5 2.19,
P40.05; surrogate cling: F(1, 95) 5 2.66, P40.05).
Home-cage behavior was influenced by age: environmental exploration
increased (F(3, 285) 5 15.61, Po0.001), while surrogate clinging and selfmouthing decreased (cling: F(3, 285) 5 13.55, Po0.001; self-mouthing: F(3,
Am. J. Primatol. DOI 10.1002/ajp
Early Predictors of Self-Biting / 589
285) 5 7.06, Po0.001). Play and self-directed behaviors did not change with age
(play: F(3, 285) 5 0.65, P40.05; self-directed: F(3, 285) 5 0.68, P40.05).
DISCUSSION
In this study most self-biters were surrogate-reared, not peer-reared. It has
been shown that raising macaque infants continuously in pairs can result in
behavioral problems [Chamove et al., 1973; Ruppenthal et al., 1991], while raising
infants in larger groups results in less severe behavioral outcomes [Chamove
et al., 1973; Clarke & Snipes, 1998]. The peer-reared infants in the present study
were housed in groups of four, and the groups were provided with artificial
surrogates for additional clinging surfaces. This combination may have helped to
ameliorate the behavioral problems that were observed in earlier studies of
continuous peer housing. In addition, the present study followed the infants after
they left the nursery and, in most cases, well into adulthood.
Rates of self-directed biting have been inversely associated with cortisol
levels. In one study adult rhesus monkeys that exhibited high rates of self-biting
had lower levels of plasma cortisol [Tiefenbacher et al., 2000]. Nursery-reared
infant rhesus monkeys also had significantly lower plasma cortisol concentrations
than mother-reared monkeys, suggesting a lower ‘‘set-point’’ for the hypothalamic-pituitary-adrenocortical (HPA) axis. This difference in cortisol levels
appears to be associated with the amount of social interaction an animal
experienced, since those with less social contact had lower levels of plasma cortisol
[Capitanio et al., 2005]. When plasma cortisol was collected from infant rhesus
monkeys after a 30-min isolation period on days 90, 120, and 150, surrogatereared infants had lower cortisol levels than peer- or mother-reared infants.
However, there was no difference in cortisol between peer- and mother-reared
infants [Shannon et al., 1998]. Surrogate rearing in the nursery with
approximately 2 hr or less of social contact per day may predispose an animal
to both lower cortisol levels and an increased likelihood of self-biting.
Previous studies have reported a strong sex bias in self-biting behavior, with
males self-biting more than females [Cross & Harlow, 1965; Gluck & Sackett,
1974; Lutz et al., 2003; Suomi et al., 1971]. However, in the present study the
subject’s sex did not appear to influence the levels of self-biting. One possible
reason is the difference in the number of observations between males and
females. Because of colony management practices, the females in the present
study typically were retained longer than the males. As a result, females were
observed significantly more times than males. Perhaps if more observations were
conducted on males, more males would be reported to self-bite. Another
difference between the previous studies and the present study is how the animals
were housed. The earlier studies utilized animals that were reared in partial
isolation [Cross & Harlow, 1965; Gluck & Sackett, 1974; Suomi et al., 1971] or
were later individually housed [Lutz et al., 2003]. Approximately 25% of the
individually-housed subjects were reported to self-bite [Lutz et al., 2003]. The
animals in the present study were socially housed and had a lower percentage
of self-biting overall (6.8%). Although the percentage of self-biting females was
comparable to that of individually housed females (7.0% in the present study vs.
7.4% in Lutz et al. [2003]), the percentage of males that self-bit was much lower
than that previously observed in individually housed males (6.6% in the present
study vs. 38.7% in Lutz et al. [2003]). Males may be more sensitive to a restricted
rearing or housing condition, which puts them at a greater risk for self-biting.
Am. J. Primatol. DOI 10.1002/ajp
590 / Lutz et al.
Although the rearing method employed may play a large role in the development
of self-biting behavior, it does not explain the presence of biters and nonbiters within
a rearing condition. In the present study, surrogate-reared animals with a record
of self-biting were less social and exhibited less social clinging when in their play
groups. Perhaps these animals did not as readily utilize conspecifics for comfort
during stressful situations, and instead resorted to self-biting as a misdirected coping
response. Regardless of the underlying mechanism, lower amounts of social contact
while in the play cage may be a predictive factor for later self-biting behavior.
Although there may be a variety of causes for a single self-biting episode,
rearing condition appears to play a major role. Surrogate rearing combined with
lower levels of social contact during play may be predictive factors for self-biting
in rhesus macaques. This information can aid in the planning of rearing and
housing practices that may help to prevent, or at least minimize, the development
of self-biting behavior.
ACKNOWLEDGMENTS
The authors thank the anonymous reviewers for their constructive
comments on this manuscript. This research was supported by the Intramural
Research Program of the National Institute of Child Health and Human
Development (NICHD), National Institutes of Health (NIH).
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