Rearing condition and plasma cortisol in rhesus monkey infants

Previous studies comparing plasma cortisol levels in mother-reared and nursery-reared rhesus monkey infants under baseline and stress conditions have reported conflicting findings. Differences in subject age, procedures, and specific rearing history may account for many of the discrepant findings. In the present study, mother-reared infants from large social groups, peer-only reared animals, and infants reared with surrogates and limited peer contact were studied in different test conditions across the first 6 months of life. Infants were sampled under three conditions: following a neonatal assessment at Days 14 and 30, immediately upon capture on Day 60, and after 30-min isolation periods on Days 90, 120, and 150. Mother-reared infants exhibited higher cortisol levels on Days 14 and 30 than did both types of nursery-reared infants. In addition, Day 60 basal values of mother-reared infants were higher than those of both peer-reared and surrogate/peer-reared infants. However, on Days 90, 120, and 150, both mother-reared and peer-reared infants exhibited higher cortisol levels in response to separation and 30-min isolation than did the surrogate/peer-reared infants. These differences may reflect group-specific variations in physical environment, capture time, feeding regimen, or diurnal HPA axis rhythms. Am. J. Primatol. 46:311–321, 1998. © 1998 Wiley-Liss, Inc.     

Mirror-induced social facilitation in stumptailed macaques (Macaca arctoides)

Seven adult female stumptailed macaques (Macaca arctoides) were confronted alternately with their reflection in a mirror and with the mirror covered. The reflection elicited significantly more visual attention and social responding than the control stimulus, replicating previous findings. Mirror-image stimulation did not significantly affect the subjects' manipulation of unfamiliar objects, but it did increase bout-lengths of episodes of drinking from a bottle containing orange juice. Possible explanations for the ability of the mirror to induce social facilitation of drinking but not of object manipulation are discussed, along with possible underlying mechanisms. Mirror-induced social facilitation is further evidence that monkeys interpret their reflection as a conspecific.     

Behavior of nursery/peer-reared and mother-reared rhesus monkeys from birth through 2 years of age

The behavior of 8 nursery/peer-reared and 16 mother-only reared rhesus macaques was observed between birth and 5 months of age, with follow-up studies conducted when the animals were 10–21 months old and living in large social groups. Nursery-reared neonates were more awake, active, and irritable than mother-only reared monkeys. From 1 to 5 months of age the nursery/peer-reared animals exhibited a greater variety of behaviors than the mother-only reared infants, which spent the majority of the time in ventral contact with mothers. As juveniles the groups were indistinguishable with the exception of more self-directed behaviors observed in the nursery/peer-reared monkeys. Both rearing conditions, by virtue of their atypicality, imposed restrictions on social development. The behavioral similarity of the juveniles while in the large social group may be a function of maturation or due to the rehabilitative effect of the large social group.     

Persistent Effects of Peer Rearing on Abnormal and Species-Appropriate Activities but Not Social Behavior in Group-Housed Rhesus Macaques (Macaca mulatta)

Nursery rearing of rhesus macaques (Macaca mulatta) alters behaviors but may be necessitated by maternal rejection or death, for research protocols, or for derivation of SPF colonies. The Tulane National Primate Research Center maintains a nursery-reared colony that is free from 9 pathogens as well as a mother-reared colony free from 4 pathogens, thus affording an opportunity to assess the outcomes of differential rearing. Nursery-reared macaques had continuous contact with 2 peers and an artificial surrogate (peer rearing). Focal sampling (432 h) was collected on the behavior of 32 peer-reared and 40 mother-reared subjects (age, 1 to 10 y; immature group, younger than 4 y; adult group 4 y or older). All animals were housed outdoors in like-reared social groups of 3 to 8 macaques. Contrary to expectation, no rearing effects on affiliative or agonistic social behaviors were detected. Compared with mother-reared subjects, peer-reared macaques in both age classes had elevated levels of abnormal appetitive, abnormal self-directed, and eating behaviors and lower levels of locomoting and vigilance (highly alert to activities in surrounding environment); a trend toward reduced foraging was detected. Immature but not adult peer-reared monkeys demonstrated more enrichment-directed behavior and drinking and a trend toward more anxiety-related behavior and inactivity. No new rearing effects were detected in adults that had not been detected in immature subjects. Results suggest that modern peer-rearing practices may not result in inevitable perturbations in aggressive, rank-related, sexual, and emotional behavior. However, abnormal behaviors may be lifelong issues once they appear.Abbreviations: MR, mother reared; PR, peer rearedRearing history is an important consideration when addressing the needs of macaques in captivity. In breeding colonies, nursery rearing may be a necessary management intervention due to maternal incompetence or death and when a foster dam cannot be identified. In addition, nursery rearing may be required for specific types of research. Decades of research broadly indicate that a combination of an artificial surrogate, human interaction, and social contact with peers is the best way to rear macaques in the nursery, a strategy that will avoid the devastating effects of total-isolation rearing^12,19,20 and allow the animals to successfully integrate into and breed in larger social groups.³⁴ However, even with modern nursery-rearing practices, the behavioral and physiologic profiles of nursery-reared macaques differ from those of macaques that have been raised with their mothers in a social group. Behaviorally, nursery rearing is associated with an increased risk for developing repetitive stereotypies, self-biting, self-wounding, and noninjurious self-directed abnormal behavior.^{3,10,16,30,31,35,41} In addition, some evidence suggests that nursery rearing results in heightened anxiety^13,21,42 and lower levels of environmental exploration.⁶ With regard to social behavior, nursery-reared macaques show decreased levels of grooming, play, and social reciprocity, and the presence of companions does not appear to buffer them from stress.^26,42 In addition, nursery rearing is associated with increased fear and aggression.^27,44 Sexual and maternal deficits may occur as well.^15,17,18,38In addition to effects on behavior, physiologic changes have been identified in macaques reared in the nursery setting. Differential rearing affects brain architecture involved in cognition,³⁷ emotional processing²⁵ and vulnerability to adverse effects of stress.⁴⁰ Although evidence concerning rearing effects on the hypothalamic–pituitary–adrenal axis is equivocal, differences including reduced levels of oxytocin, norepinephrine, and homovanillic acid in the cerebrospinal fluid have been reported.^22,27,28,44 Studies have identified several indicators of immune system alterations in nursery-reared macaques, such as decreased proportions of cytotoxic and suppressor T cells, reduced natural killer cell activity, and increased lymphocyte proliferation.^9,29With regard to social management in the nursery, strategies fall into 2 main categories: peer rearing, involves continuous cohousing, whereas surrogate–peer rearing involves brief periods of cohousing of otherwise singly housed infants. Although infants in both rearing conditions may be provided an inanimate surrogate, surrogate–peer-reared infants are housed for the majority of the time with the inanimate surrogate only, with the intention that infants’ need for clinging to an attachment figure will be directed toward the surrogate, even when peers are present. However, this distinction is generalized, and both nursery-rearing categories may involve variations across facilities. Moreover, a subset of the literature differentiates between these housing conditions and compares them. In comparison with surrogate–peer rearing, peer rearing is associated with lower levels of stereotypic and self-injurious behavior, ^31,35,36 whereas surrogate-peer rearing appears to mitigate the increased anxiety observed in peer-reared subjects.^12,20,40 In addition, surrogate–peer-reared macaques show less social clinging, fear, and aggression and more exploration and play than do their peer-reared counterparts.^5,7,35,36Although the literature on the nursery rearing of macaques is extensive, many of the studies concerning the behavioral effects of rearing involve both infants and older subadults or evaluations of behavior indoors and under test conditions. Therefore these populations need to be characterized more thoroughly under the conditions in which they are housed. The relative costs and benefits of the 2 forms of nursery rearing may vary with time and housing condition, especially when the ultimate goal is to maintain the animals long-term and for breeding purposes. For example, nursery-reared macaques may be eventually housed in small outdoor groups, particularly as part of the process of deriving SPF colonies,³⁸ and the literature in the context of their behavior in a more naturalistic group setting is sparse.The question of which nursery rearing practice optimally equips macaques with species-normative behaviors to live in an outdoor group-housed situation is best assessed by comparing mother-reared, peer-reared, and surrogate–peer-reared subjects in similar physical and social conditions. However, even when all 3 categories of animals are unavailable, comparing mother-reared with peer-reared macaques is valuable for assessing the downstream consequences of nursery-management decisions. The objective of the current study was to characterize the behavior of peer-reared, outdoor group-housed rhesus macaques compared with that of mother-reared, outdoor group-housed subjects. Although we expect broad social and reproductive competence in these animals, we test the prediction that peer rearing results in significant perturbations in social behavior as well as heightened anxiety. Characterizing this population is necessary for determining its behavioral needs. If the long-term effects of rearing mimic signs of current reduced wellbeing, it is difficult to assess the need for intervention and the expected response to that intervention. This assessment will allow us to measure the cost of management decisions designed to mitigate rearing-related abnormal behaviors, to predict or interpret the behavior of breeding groups consisting of peer-reared macaques, and ultimately, to contribute to the literature that may guide our ability to make evidence-based decisions regarding different nursery-rearing strategies. Furthermore, this study uses subjects of widely varied ages in both rearing categories to gain information on the long-term stability of rearing differences with increasing age.     

Social responding to mirrors in rhesus macaques (Macaca mulatta): Effects of changing mirror location

Two rhesus macaques (Macaca mulatta) with a lifetime of continuous exposure to mirrors showed a dramatic and reliable reinstatement of social behavior directed toward the mirror when it was simply moved to a new location. These data are discussed in the context of repeated failures to find self-recognition in monkeys and several recent claims that a cessation of social behavior directed toward mirrors can be used as evidence for the beginning of self-recognition in nonhuman primates.     

Social stimuli as incentives for delayed response performance by infant pigtailed macaques (Macaca nemestrina)

Six pigtailed macaque monkeys (Macaca nemestrina), ranging in age from 4.5 to 13.5 months, were studied longitudinally on a delayed response procedure in a spatial choice apparatus. In each trial the subjects were exposed to two stimulus animals, an unfamiliar adult female and a familiar age-mate. Prior work showed that such nursery-reared infants overwhelmingly prefer a familiar peer over an unfamiliar adult female. Therefore, the peer was considered to be a positive incentive and choosing the peer was defined as the “correct” response. After the infants were given visual exposure to the stimulus animals, an opaque door was lowered to block them from the subject's view. Then a single delay period of 0, 5, 15, 60, 120, 240, or 480 sec was introduced during 20-trial sessions. The delays were increased over sessions, with about two weeks between sessions. The subjects reliably chose the familiar peer after delays of up to 60 sec, with one subject maintaining correct choices even after 8-min delays. These results revealed that the delayed response performance of young macaques with social incentives was as good as, or better than, maximum performance levels reported for macaques with food incentives. Cues such as odors, sounds, and visual-postural orientation sets could not explain the performance levels at long delays found in this study.     

Responses to animal stimulus photographs in stumptailed macaques (Macaca arctoides)

Interest in their animate environment was studied in a captive group of 11 stumptailed macaques (Macaca arctoides). Subjects were shown projected photographic slides, most of which showed a single individual primate or non-primate. The measure of interest was the duration of viewing. Results showed that adult females exhibited more interest towards stumptailed macaques versus other macaques species, and towards adult females carrying infants versus adult females alone. Data concerning non-primates showed that subjects were especially interested by photographs of felids; this effect was partly due to the presence of two frontal and conspicuous eyes in felids.     

Early behavioral development and temperamental traits in mother- vs peer-reared rhesus monkeys

Behavioral characteristics (“traits”) of 24 mother-reared and 24 nursery/peer-reared rhesus monkey infants were assessed via rating scales from the third through the seventh month of life while housed with their rearing partners, and from months 8–10 after all animals had been placed in novel peer groups. The animals were also tested at 8 months of age on the Bayley Scales of Infant Development adapted for nonhuman primates. During the early period effects noted were primarily developmental. Peer-reared animals were rated as increasingly less cautious and more attentive to the outside environment over time, while mother-reared infants declined in ratings of dependence on their mothers. All animals were rated as increasingly active and excitable, and less fearful, over time. For the period of months 8–10, peer-reared animals showed higher confidence ratings in month 10, and all animals showed a decline in attachment to cagemates. Mother-reared animals showed more hostility to the examiner during Bayley testing, whereas peer-reared animals showed more fear. Sex effects included greater ratings for independence from mothers, greater activity over both the early and later periods, greater excitability, greater attentiveness to the extra-cage environment, less cautiousness, and better performance on one Bayley problem for females.     

Peer-rearing influences subsequent maternal behavior and infant survival in a newly formed herpes B-virus negative rhesus macaque group

The maternal behavior of primiparous rhesus macaques (Macaca mulatta), peer-reared since 1/2 years(s) of age as part of aHerpesvirus simiae (herpes B-virus) screening protocol, was examined and compared to a control group of conspecifics reared in their natal group. Infant survival was significantly higher in control groups as compared to the test group, a result attributed to the high incidence of infant kidnapping/abandonment in the test group. Among the test subjects, infant survival rate increased as the birth season progressed, thus it is possible that exposure to mothers/infants helped in the maternal success of those females who gave birth later in the season. Test group infants were touched by group members significantly more than the infants of control subjects, whereas these infants were groomed by their mothers and in a ventral position for a greater time relative to the infants of the test subjects. This study suggests that females, partially reared in peer groups, may be at early risk for maternal incompetence and consequent greater infant mortality, and that exposure to mother-infant dyads may augment the proficiency of maternal skills.     

Social context and reaction to separation in peer-reared pigtail macaques: Some preliminary observations

The social environment affects both behavioral and physiological responses to separation from the mother. Less information is available on the impact of the social environment on the response to separation in peer-reared infant monkeys. This study reports the responses of peer-reared pigtail macaque infants to repeated separations, and the impact of social versus isolation housing during the separation. The responses of two pairs of monkeys were studied during four three-day separations. One of each pair was housed in isolation during the separation, and the other was with another pair of peers, with whom they had been living for one month prior to the separation. The isolation-housed peer responded to the separation with behavioral agitation, but no depression. The socially-housed peer's behavior did not differ from baseline during the separation. During successive reunions, all the separated monkeys, regardless of housing condition, exhibited declining levels of behaviors related to maintaining proximity to their attachment figure. Although the number of subjects is small, the results suggest that the presence of social support, in the form of a familiar peer, can ameliorate the response to separation, and that with repeated separations the responses of the monkeys changes significantly.     

Self-aggression in stumptail macaques: Effects of frustration and social partners

This study aimed to test the hypotheses that frustration and low social status are associated with increased levels of self-aggression (SA) in stumptailed macaques. SA was more frequent when adult macaques observed from an adjacent cage while a companion was being tested on a memory task than when they themselves were tested. Watching a companion being fed by a human also caused SA to increase when subjects were alone, but not when they were with another partner. Overall, the subject of intermediate dominance rank appeared the most prone to bouts of SA. The results are discussed with reference to the role of frustration and social status in SA, and it is concluded that social housing with compatible partners can reduce this abnormal behaviour.     

Pair-rearing infant monkeys (Macaca nemestrina) using a “rotating-peer” strategy

Appropriate rearing conditions for captive primates are important for both research and breeding purposes. In an earlier study, pigtailed macaque infants that were pair-reared with a single continuous partner exhibited excessive social clinging and could not adapt to living in large social groups at 8–10 months of age. In the present study, eight macaques were pair-reared until they were 6 months old. Each member of an animal's four-monkey social group served as a home-cage partner. In an attempt to reduce excessive mutual clinging, the pairs were rotated every 2–3 days to increase the variability of social stimulation in the home cage. However, these infants developed abnormal social behaviors that were in some cases even more extreme than those exhibited by infants pair-reared with a single continuous partner. A second goal of this experiment was to study interlaboratory reliability for the development of social behavior. The animals were divided into two groups, one housed in a nursery and the other in a biological safety level 3 virus laboratory. Some differences were detected between the two groups, demonstrating the necessity of controls in biobehavioral developmental research. Am. J. Primatol. 41:141–149, 1997. © 1997 Wiley-Liss, Inc.     

Mirror-image responses in pygmy marmosets (Cebuella pygmaea)

Only a few nonhuman species (chimpanzees and orangutans) have displayed mirror-image recognition of themselves by grooming at a spot that can only be seen with the mirror. Pygmy marmosets have never been observed to self-groom, but they do behave toward mirrors in a manner suggestive of the early stages of mirror-image recognition. They displayed a rapid extinction of social threat responses to their own image and of novelty responses to mirrors, but continued to show mirror-specific responses such as following their own image, playing peek-a-boo, and looking at their image throughout a 28-day period of mirror exposure. The pygmy marmosets used a mirror to locate otherwise unseen conspecifics from other groups and directed threat responses toward the real location of these animals rather than to their mirror-image. Pygmy marmosets displayed the precursor behaviors to mirror-image recognition.     

Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta)

Studies on early development have demonstrated the profound effects of early social experience on the behavioral development and physiology of young rhesus macaques. Given these relationships, we hypothesized that rhesus macaques exposed to different nursery-rearing conditions may develop unique biobehavioral profiles. If this is true, the assessment of temperament may allow us to pinpoint successful rearing environments, thus improving the overall health of nonhuman primates that are raised in captive environments. We conducted biobehavioral assessments in order to examine differences in the development of infants raised under four different peer-rearing conditions (continuous pairing (CP), intermittent pairing, CP with partner rotation, and intermittent rotational pairing) and compared these animals with data from a mother-reared control group. Overall, continuous rotationally paired animals were most similar to mother-reared controls on most behavioral and temperament measures, suggesting that more socially complex rearing environments (greater number of social partners) favor a more active behavioral style. Cortisol profiles of mother-reared controls were similar to both CP groups, and these three groups had higher cortisol concentrations than the intermittent rotational-pairing group. In addition, intermittently paired infants displayed a significantly higher frequency of self-stroke behavior during a human intruder challenge, an abnormal behavior also known as floating limb which has been shown to be a precursor of self-biting. Overall, the data are consistent with the idea that social complexity in the nursery, as operationalized in our continuous rotational pairing, leads to a biobehavioral profile that is most similar to that of infants raised by their mothers in large, socially complex, cages.     

Modulation of anxiety-related behaviors by mu- and kappa-opioid receptor agonists depends on the social status of mice

This study was aimed to determine the effects of mu- and kappa-opioid receptor activation in relation to the social status of mice, being a winner with repeated experience of victories or a loser with repeated experience of social defeats. The behaviors of the animals were assessed in a social encounter test measuring the communicative behavior towards a familiar and an unfamiliar partner behind a perforated transparent partition (partition test) and in an elevated plus-maze test estimating the anxiety level of mice. Placebo and graded doses of the mu-opioid receptor agonist DAMGO (0.5 and 2 mg/kg s.c.) and the kappa-opioid receptor agonist U-50,488H (0.6, 1.25, and 2.5 mg/kg s.c.) were administered to the control mice, winners and losers in two experiments. In the partition test, the winners spent somewhat more time and the losers less time than the controls in the vicinity of their partner probably related to a lower and higher level of anxiety respectively. In the plus-maze test the losers appeared to have a somewhat higher anxiety level than the controls and winners. In both tests DAMGO produced anxiogenic-like effects in the winners and the controls, but not in the losers. Winners hardly responded to treatment with U-50,488H, while the losers responded dose dependently with an anxiolytic-like effect in both tests. It is concluded that anxiety-like responses in mice are differentially affected by stimulation of mu- and kappa-opioid receptors and that the effects depend on the social status of the animals.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Dispersal,nepotism, and primate social behavior

High degrees of relatedness within primate social groups are thought to promote the evolution of altruistic behavior via kin selection. Dispersal, for whatever reason, should limit opportunities for nepotistic behaviors. Conversely, emigration is usually attributed to the avoidance of inbreeding depression. Actual dispersal patterns may result from a balance of these forces. Systematic behavioral differences are expected between taxa that differ in such patterns. In fact, comparisons of (a) colobines vs. cercopithecines, (b) bonnet, stumptailed, and Barbary macaques vs. Japanese and rhesus macaques, and (c) red vs. mantled howler monkeys yield a perplexing blend of unexplained differences and unmet theoretical expectations. Kin selection may be less important than generally believed, and/or methodological standardization more so.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

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

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=183), peer-reared in groups of four (n=84), and surrogate-peer-reared (n=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, surrogate-peer-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.     

The structure of affiliative relations in a primate community: Allogrooming in stumptailed macaques (Macaca arctoides)

Social grooming in 19 adult stumptailed macaques (a dominant male and 18 females) was studied by focal sampling and scanning methods. Significant individual differences were found with respect to both active and passive grooming intensity, active grooming being a more variable parameter. Individual preferences in partner choice are very strong, but among the factors examined, age was the only one influencing these preferences. Neither social rank nor kinship were significant. The proportion of active and passive contacts shows marked individual differences. Yet, there is a positive association between performed and received grooming. The “extortion hypothesis” is not supported by our results: high-ranking individuals performed on the average more, and received relatively less grooming than low-ranking ones. High grooming performance of the dominants may secure group integrity in species with a “soft” dominance style.