Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta).код для вставкиСкачать
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: firstname.lastname@example.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. ), 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. ). 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. 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