Improved behavioral indices of welfare in continuous compared to intermittent pair-housing in adult female rhesus macaques (Macaca mulatta)

Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.     

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.     

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.     

Effects of age,rearing, and separation stress on immunoglobulin levels in rhesus monkeys

The study reported here examined the effect of different rearing conditions and psychological stress on immunoglobulin levels in rhesus monkey infants. In the first experiment, 24 rhesus neonates were placed in one of the three following rearing conditions: Separated from their mothers and reared in the laboratory nursery; kept with their biological mothers; or removed at birth from their biological mothers and cross-fostered to adoptive rhesus mothers. Plasma samples were obtained from the nursery-reared infants immediately after birth and at weekly intervals for the next 30 days. Samples were also obtained from mother-reared and foster-reared infants on days 15 and 29. All samples were tested for IgG and IgM levels. The results indicated that neither rearing nor diet affected Ig levels. IgG levels were highest at birth and decreased progressively for the first 30 days, suggesting that placental transfer of maternal IgG is the critical determinant of IgG levels in primate infants as in humans. IgM changes were also similar to those in human infants: Low levels at birth, a significant increase from birth to day 15, and a moderate decline from day 15 to day 30. When IgG levels and IgM levels were correlated across the first month, many significant correlations were found which were consistent with human data relating both infant IgG and IgM levels to infant maturation. In the second experiment, 11 of the previously tested nursery infants were subjected to four consecutive social separations from peer groups at 6 months of age. Plasma samples were obtained before and after the first and fourth weeks of separation and tested for IgG and IgM levels. Small but significant decreases in both immunoglobulins were detected after 4 days of separation, particularly on the fourth week.     

Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

Motherless mothers revisited: Rhesus maternal behavior and rearing history

Classic studies have demonstrated that isolation- and peer-rearing in infancy can result in overt deficits in maternal behavior in rhesus monkeys, although nonmother-reared monkeys may become adequate caretakers if allowed experience with infants. Maternal styles in normally-reared mothers have been reported to vary widely. In the present study, the range of maternal proficiency of nonabusive, nonrejecting nonmother-reared mothers was examined. The behavior of mother-reared, peer-reared, and isolate-reared multiparous mothers was observed and compared for the first six months following parturition. Both peer-reared and isolate-reared mothers exhibited differences in maternal behavior from mother-reared mothers. Inasmuch as variations in maternal behavior may impact on the infant, investigators should be aware of the rearing histories of females used as breeders in the laboratory.     

Separation of preadolescents from infant rhesus monkeys

Each of eight infant rhesus monkeys was paired with a preadolescent conspecific for two months and then separated. Four of the infants were mother-reared and four were isolate-reared. Separation responses were compared with data from preseparation and reunion phases of the study for all pairs. The results indicate that (1) although males interact with infants in a parental fashion, preadolescent females show a greater capacity for parental behavior, (2) both preadolescents and normal (mother-reared) infants contribute to the development of a social bond, (3) isolate infants contributed little to the development of a social bond and were relatively less-valued as social partners by their preadolescent cagemates.     

Factors predicting increased incidence of abnormal behavior in male pigtailed macaques

To identify factors predicting abnormal behavior in laboratory monkeys, we observed all available singly housed 4- to 11-year-old male pigtailed macaques (Macaca nemestrina), the species/age/sex group most likely to be referred to the Washington National Primate Research Center's Psychological Well-Being Program for behavioral assessment. Of the 87 subjects, 29 had been referred to the program whereas 58 had not. Abnormal behavior was unrelated to the subject's housing location (biocontainment vs. other facility) or invasiveness of research. Nursery-reared subjects displayed more abnormal behavior than mother-reared subjects. Across and within rearing categories, the proportion of the first 48 months of life spent singly housed was positively related to the amount of abnormal behavior at maturity. This effect was stronger for subjects separated from the mother for clinical rather than experimental reasons, and least for mother-reared subjects. Locomotor stereotypy, by far the most frequent form of abnormal behavior, was positively related to time in single housing but was unrelated to rearing. These results reinforce the importance of tactile social contact during juvenility for the prevention of abnormal behavior in social primates. They also suggest that self-directed abnormal behaviors and locomotor stereotypies have different etiologies.     

Hormonal effects of early rearing conditions in the infant rhesus monkey

Mother-reared and nursery-reared rhesus monkeys were evaluated during the first month of life to assess the effects of early rearing on endocrine status in infancy. Plasma cortisol and growth hormone (GH) levels were measured in two conditions: (1) basal and (2) 30 min following removal from either the mother or the nursery. Nursery-reared infants had lower basal GH levels and higher cortisol levels than did mother-reared infants. Both GH and cortisol levels rose significantly following separation and reached similar levels in the mother-reared and nursery-reared infants. Mother-reared animals exhibited higher GH levels in response to a pharmacological GH-stimulation test. Thus nursery rearing of primate infants significantly affected the baseline secretion of two important endocrine systems, but did not appear to alter markedly the acute endocrine response to a psychological stressor.     

Serotonin transporter expression is predicted by early life stress and is associated with disinhibited behavior in infant rhesus macaques

Serotonin transporter (5-HTT) expression patterns may contribute to the risk for adverse psychological outcomes following early life stress. The present study investigated whether two types of early life stress, maternal and social aggression, and a serotonin transporter gene promoter polymorphism ( rh5-HTTLPR ) predicted lower post-stressor peripheral blood mononuclear cell (PBMC) 5-HTT expression in infant rhesus macaques. We further probed the relationships among these factors and infant behavioral disinhibition within a stressful situation. Fifty-three infants residing with mothers in large, complex social groups were observed over the first 12 postnatal weeks, during which time the rate of aggression received by the infant from their mothers and social group members was recorded. At 90–120 days of age, infants underwent a 25-h maternal separation/biobehavioral assessment, which included standardized behavioral assessments and blood sampling. Infants' rh5-HTTLPR genotypes were determined, and infant 5-HTT expression was quantified from PBMCs collected 8 h after separation. Receipt of aggression from the mother, but not from social group members, was associated with lower post-stressor 5-HTT expression. Lower post-stressor 5-HTT expression, but not receipt of aggression, was associated with disinhibited behavior during assessment. Rh5-HTTLPR genotype was unrelated to any measure. We conclude that 5-HTT regulation is linked with specific, presumably stressful early experiences in infant rhesus macaques. Further, 5-HTT expression predicted behavioral disinhibition, presumably via parallel processes that operate in the brain.     

Growth and development of infant giant pandas (Ailuropoda melanoleuca) at the Wolong Reserve,China

From 1991 to 1993 inclusive, seven infant giant pandas (Ailuropoda melanoleuca) were born at the China Conservation and Research Center for the Giant Panda. Average daily weight gain in the first 6 months for mother-reared infants (n = 5) was 71.3 g/day; for one partially mother-reared and partially hand-reared infant, 41.5 g/day; and for one completely hand-reared infant, 50.3 g/day. There was a significant difference in growth rates across the first 6 months in all methods of rearing. In addition, a comparison of growth rates across the three rearing methods showed significant differences in the first, second, third, fifth, and sixth months. Average daily body length increase for mother-reared infants was 4.1 mm/day; for partially mother-reared/partially hand-reared infants, 4.0 mm/day; and for the completely hand-reared infant, 2.8 mm/day. In mother-reared infants, body length increase during the first month was significantly greater than during the following months, and was slowest during the sixth month. At birth, infants were all pink in color with a light white coat of lanugo. Black pigmentation was first noted at 7–10 days of age, which was also the time that initial hair coat growth was seen. Eyes opened at 35–48 days of age. Ears opened at 31–50 days of age. Deciduous dentition was first seen at 82–121 days of age, while permanent dentition began to erupt at 350 days of age. © 1996 Wiley-Liss, Inc.     

Successful behavioral strategy to unite mother and infant rhesus monkeys (Macaca mulatta) after cesarean delivery

Developmental studies of pre‐ to postnatal continuities in rhesus monkeys sometimes require infants be reared with their mothers. However, complications during pregnancy or experimental designs may require cesarean delivery. Owing to lack of published information on this subject, strategies are needed to introduce mothers to their infants following cesarean delivery. Using positive and negative reinforcement techniques we attempted to unite six infant rhesus macaques, Macaca mulatta, to their mothers following c‐sections. For our seventh subject, we attempted to cross‐foster an infant onto an unrelated female after she had undergone a cesarean surgery for a late‐term spontaneous abortion. The mothers varied in age, parity, previous postnatal mothering experience with infants, housing earlier to delivery, and housing subsequent to introduction. Although there were large individual differences among the mother–infant pairs, all seven introductions were successful. The mothers learned to accept and care for their infants from the continuous application of operant conditioning techniques. These data suggest that mother‐rearing following cesarean section is a realistic possibility whether required for clinical reasons or for proper experimental control. Furthermore, the ability to successfully mother‐rear infants produced from cesarean delivery lessens the impact this potential confound of not being reared by their mothers exerts on many types of developmental studies. Am. J. Primatol. 71:510–522, 2009. © 2009 Wiley‐Liss, Inc.     

Infant stumptailed macaques reared with mirrors or peers: Social responsiveness,attachment, and adjustment

Comparisons of activity toward mirrors and peers in infant macaques being reared with one of these stimuli as the primary rearing partner revealed markedly greater social responsiveness to a fully accessible cagemate than to one's own reflection. Measures of exploration, aggression, and especially play all revealed the cagemate to be the more potent social stimulus. Mirror-reared infants given additional experience of a live peer behind a transparent partition were less responsive to the mirror than were infants with no social stimulation other than a mirror. In contrast, cagemate-directed behavior of peer-reared infants was not seriously affected by additional exposure to a mirror. A fully accessible peer also elicited more social responding than a peer behind a transparent partition, and infants with experience of both a live cagemate and mirrors were generally more responsive toward the former. Greater agitation in peer-reared than in mirror-reared stumptailed monkeys during separations from their rearing partners suggests that exposure to the physically accessible partner led to stronger attachments. Infants reacted positively to a moderately unfamiliar environment but showed behavioral disruption when placed in a very unfamiliar environment. Disruption was especially evident in peer-reared infants, in which exposure to the unfamiliar environment was compounded with the absence of the attachment figure. Mirror-rearing appeared to reduce the tendency toward ‘isolation syndrome’ behaviors compared to alone-rearing, and these behaviors appear to be less common in stumptailed than in rhesus macaques.     

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.     

Temperament in Rhesus,Long‐Tailed,and Pigtailed Macaques Varies by Species and Sex

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey—rhesus (Macaca mulatta), long‐tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques—using cage‐front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early‐life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long‐tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species’ social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male–male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species‐typical behaviors adaptive. Our results suggest that adaptive species‐level social differences may be encoded in individual‐level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303‐313, 2013. © 2012 Wiley Periodicals, Inc.     

Effect of Mother's Dominance Rank on Offspring Temperament in Infant Rhesus Monkeys (Macaca mulatta)

In humans, temperament plays an important role in socialization and personality. Some temperaments, such as behavioral inhibition are associated with an increased risk for psychopathology. Nonhuman primates can serve as a model for neurobiological and developmental contributions to emotional development and several recent studies have begun to investigate temperament in nonhuman primates. In rhesus monkeys, dominance rank is inherited from the mother and is associated with social and emotional tendencies that resemble differences in temperament. The current study assessed differences in temperament in infant rhesus monkeys as a function of maternal dominance rank. Temperament was assessed in 26 infants (13 males) from birth until 6 months of age with a battery that included Brazelton test, human intruder test, human intruder‐startle, cortisol stress reactivity, and home cage observations of interactions with peers and the mother. Throughout testing, infants lived with their mothers and a small group of other monkeys in indoor/outdoor runs. Dominance rank of the mothers within each run was rated as either low/middle (N = 18, 9 male) or high/alpha (N = 8, 4 female). Infants of high‐ranking mothers displayed more intruder‐directed aggression and reduced startle potentiation in the human intruder tests. Dominant offspring also had reduced levels cortisol and startle across development and spent more time away from mothers in the interaction tests. These results suggest that dominance of the mother may be reflected in behavioral reactivity of infants early in life. These findings set up future studies, which may focus on contributing factors to both dominance and temperament such as genetics, rearing, and socialization. Such factors are likely to interact across development in meaningful ways. These results also suggest future human‐based studies of a similar relationship may be warranted, although social dominance is clearly more complex in human than macaque societies. Am. J. Primatol. 75:65‐73, 2013. Published 2012 by Wiley Periodicals, Inc.?     

Paternal early experiences influence infant development through non-social mechanisms in Rhesus Macaques

Background

Early experiences influence the developing organism, with lifelong and potentially adaptive consequences. It has recently become clear that the effects of early experiences are not limited to the exposed generation, but can influence physiological and behavioral traits in the next generation. Mechanisms of transgenerational effects of parental early experiences on offspring development are often attributed to prenatal or postnatal parental influence, but recent data suggest that germ-line plasticity may also play a role in the transgenerational effects of early experiences. These non-genetic transgenerational effects are a potentially important developmental and evolutionary force, but the effects of parental experiences on behavior and physiology are not well understood in socially complex primates. In the non-human primate, the rhesus macaque, nursery rearing (NR) is an early life manipulation used for colony management purposes, and involves separating infants from parents early in life. We examined the effects of maternal and paternal early NR on infant rhesus macaque immunity, physiology, and behavior.

Results

We theorized that differences in behavior or physiology in the absence of parent-offspring social contact would point to biological and perhaps germ-line, rather than social, mechanisms of effect. Thus, all subjects were themselves NR. Male and female infant rhesus macaques (N= 206) were separated from parents and social groups in the first four days of life to undergo NR. These infants differed only in their degree of NR ancestry – whether their dams or sires were themselves NR. At 3-4 months of age, infants underwent a standardized biobehavioral assessment. Factors describing immunity, plasma cortisol, and emotion regulation were generated from these data using factor analysis. Paternal, but not maternal, NR was associated with greater emotionality and higher plasma cortisol, compared with infants born to CONTROL reared fathers.

Conclusions

These data suggest that macaque biobehavioral makeup is strongly influenced by paternal experiences, and via non-social mechanisms.

     

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.     

Psychological well-being in paired adult female rhesus (Macaca mulatta)

We assessed the effects of social living (pairing) on improving the psychological well-being of adult female rhesus macaques (Mucuca mulutta) housed under laboratory conditions. We measured well-being in 12 pairs and 12 singly housed females through multiple indices of health (hematology, clinical morbidity, and body weight), stress (immune responses), behavior (preferences for social proximity, exhibition of species typical affliative behavior, and rates of abnormal behavior), and reproduction (frequency of ovulation, rates of conception, and infant survival). We selected adult females that had been living in single-unit cages and paired them in larger cages. Care was taken to allow females to become familiar with one another before pairing took place, and pairs that fought were separated before serious injuries occurred. Singly-housed control females were also paired for 1 week and then separated to balance the stressful effects expected to occur during the initial pairing and to assure that they were equivalent to the experimental animals in their ability to live socially. We concluded that pairing adult female rhesus monkeys was a positive experience for both the dominant and subordinate members of the pairs. They chose to spend the majority of their time involved in amicable social interactions, were more active, and they indulged in less nail biting than singly-housed controls. There were no differences in reproduction, rates of clinical morbidity, or immune stress responses among the groups. However, pairing alone may not be sufficient to assure the well-being of laboratory-housed rhesus macaques, because rates of abnormal behaviors such as stereotyped movements remained high. © 1994 Wiley-Liss, Inc.     

Weight gain in captive chimpanzee infants: Comparisons by sex,rearing, and colony

Weight gain has been monitored for 13 years in a mixed longitudinal study of captive chimpanzee growth and development. This report presents results of a comparative analysis of weight relative to age in 175 animals during the first 24 months in four sex/rearing groups (hand-reared females, hand-reared males, mother-reared females, and mother-reared males) from three colonies with different physical, nutritional, and social environments (Primate Foundation of Arizona, University of Texas M.D. Anderson Cancer Center Department of Veterinary Resources, Bastrop, TX, and White Sands Research Center, Alamagordo, NM). The Lowess method is used to generate fits of weight vs. age for each group and colony, with which individual animals at these and other colonies may be compared for assessment of developmental status. Comparisons of the curves, using the jackknife approach, show that there are significant differences between the curves, indicating that rearing and environmental parameters may be factors in weight gain rate and must be considered in such an assessment. Rearing effects may be the dominant of these factors in weight gain. © 1996 Wiley-Liss, Inc.