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.     

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 rearing on aggression and subordination in papio monkeys

The objective of this study is to assess the effects of short-term maternal deprivation (birth to 12 weeks) followed by peer group rearing on the development of aggressive and subordinate behaviors in papio monkeys (superspecies – Papio cynocephalus). Nursery reared monkeys (34 males and 30 females) were compared with mother-peer reared monkeys (11 males and 12 females) in late infancy (6 to 12 months of age) and at the end of their juvenile stage (36 to 42 months of age) in social groups composed of 75% nursery reared subjects and 25% mother reared subjects. Focal animal data were analyzed with a repeated measure ANOVA model. In general, the nursery reared infants tended to be less aggressive than mother-peer reared infants and performed less dominance behaviors, such as displace. Significant sex differences were present in the performance of aggressive (♂ > ♀) and subordinate (♂ > ♀) behaviors. Significant age differences were observed, with infants having consistently higher rates of performance.     

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.     

Injury risks among chimpanzees in three housing conditions

Meeting the psychological needs of chimpanzees (Pan troglodytes) can be a challenge given their aggressiveness on the one hand and the complexity of their social lives on the other. It is unclear how to balance the need to provide opportunities for species-appropriate behavior against potential risks of injury chimpanzees may inflict on each other. This study evaluates the suggestion that simpler social environments protect chimpanzees from wounding. Over a two-year period all visible injuries to 46 adult males, 64 adult females, and 25 immature chimpanzees were recorded at the Yerkes Regional Primate Research Center. Approximately half of the subjects were mother-reared, and the rest were nursery-reared. Housing included compounds containing about 20 chimpanzees, interconnected indoor-outdoor runs for groups of up to 12 individuals, and smaller indoor-outdoor runs for pairs and trios. Annual wounding rates were calculated for serious wounds (extensive injuries and all those requiring veterinary intervention) as well as for minor wounds. Compound-housed chimpanzees incurred the highest level of minor wounding, but serious wounding levels were not affected by housing condition. Even with a period of dominance instability and elevated levels of wounding in one compound, compound chimpanzees were not injured more than those in smaller social groups over the long term. Nursery-reared females in moderate-sized groups were wounded more than mother-reared females. Also, nursery-reared males and females were wounded less often when paired with mother-reared companions. Overall, this study indicates that maintaining chimpanzees in pairs and trios would not be an effective means for reducing injuries. The management of wounding in chimpanzee colonies is influenced more by the sex and rearing composition of a colony.     

Social and reproductive behaviors in surrogate-reared squirrel monkeys (Saimiri sciureus).

A colony of 16 surrogate-reared squirrel monkeys was observed for the adequacy of social and reproductive behaviors at maturity. Aside from some self-directed abnormalities centering around nonnutritive orality, this group was behaviorally normal in spite of having no contacts with mother-reared, older conspecifics. Half (N=5) of the females gave birth, with four infants viable. One infant has remained with the colony and is thriving. The other three remained with the group for as long as 42 days before death or removal. Maternal care appeared adequate. Mean estimated conception age for females was 35 months, and the mean impregnation age for males was estimated to be 42 months.     

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.     

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.     

The development of grooming,sociosexual behavior,play and aggression in captive baboons in their first two years

This paper focuses on the development of behavior in a mixed-longitudinal sample of 77 baboons (Papio sp. — 46 males and 31 females) from birth to 2 years of age. Eleven behaviors measured as frequency of performance and frequency of reception were used to test null hypotheses of gender and rearing differences among thePapio sp. subjects. The behaviors measured included: groom, mount, present, open-mouth threat, hard bite, displace, avoid, grapple, play bite, charge and chase. The data indicate that gender differences exist in the development of grooming, sociosexual behavior and aggression and play. The data also indicate that subjects raised in the nursery environment were behaviorally indistinguishable from mother-reared peers on the basis of the 11 behavioral criteria.     

Breeding and rearing squirrel monkeys (Saimiri sciureus) in captivity.

A breeding colony of squirrel monkeys (Saimiri sciureus) was established to provide animals for behavioral research concerned with early development. The origin of the initial breeders was Peru, Colombia, and Bolivia. During the past 10 years, the colony has grown to 125 adult females, 20 adult males, and 120 immature animals of various ages. The annual conception rate for the last 5 years averaged 68%. This resulted in 84% viable births of which 82% survived past 6 months of age. The majority of the births (65%) occurred during June-August, and 87% during May-September. The most efficient and successful breeding strategy was to form mixed-sexed groups of 10--15 females and 2--3 males before the mating season began and to maintain the integrity of these groups with minimal interference. Progeny were reared apart from their natural mother without difficulty, and their growth and development were found to be similar to those of mother-reared monkeys.     

Early rearing experiences and the performance of affinitive and approach behavior in infant and juvenile baboons

We tested the hypothesis that subtle, short-term (birth to 3 months) differences in rearing experiences (peer-peer vs. mother-peer) produce measurable differences in the development and performance of four affinitive and four approach behaviors in late infancy (12 months of age) and in the late juvenile period (42 months of age). Data on 87 monkeys (45 males and 42 females) were obtained by a series of approximately 2,100 focal animal sampling sessions. Significant effects of rearing were found in two affinitive behaviors (Allogroom andHold) with mother-peer reared subjects having a higher mean rate of performance. There were no significant main effects or interactions among any of the approach behaviors. Several suggestions are proposed to account for the resistance of six behaviors (Muzzle-muzzle, Touch, Ear flatten, Follow, Lip smack andSocial approach) to the effects of the experimental procedures: (1) these behaviors may reflect genetically mediated behavioral characteristics of the species that are not modified by environmental conditions; (2) environmental conditions used in the study may have been too subtle and consequently insufficient to produce an effect on relatively resistant behaviors; or (3) effects of the early rearing experience on these behaviors may be observable only during adolescence or adulthood when the proper performance of these behaviors is more crucial to social success, social integration and reproduction. Formerly Southwest Foundation for Research and Education.     

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.     

The range of action of the mother and the avoidance of big novel objects in long-tailed macaques

Most surrogate-reared long-tailed macaques persistently avoid a big novel object, whereas most mother-reared subjects approach it. A striking difference between these attachment figures is that the mothers moved about with their infants, whereas the surrogates were fixed to the wall In this experiment, we aimed to find out whether mobility of the attachment figure plays a part in the development of an infant’s responses to big novel objects. We studied the effects of mobility of the attachment figure by restraining mothers in their range of action. We confined mothers of the experimental group in a small part of the home cage. Their infants could leave the cage in which their mothers were restrained. Infants that were growing up with unrestrained mothers made up the control group. At two different ages all infants encountered a big novel object. We used two different objects. We found that the range of action of the mother did not significantly affect the responses of infants to big novel objects. As in the previous studies, most of the mother-reared monkeys approached the objects. The age at which an infant was first exposed to an object did not significantly affect its behavior toward it. Further, the two different objects evoked the same reactions.     

Bed-building in captive chimpanzees (Pan troglodytes): the importance of early rearing

In the wild, great apes sleep in beds they make by successively bending branches into an interwoven platform. These beds are functionally more closely related to human beds than they are to the nests and tree-holes used by other primate species. The idea that bed-building by great apes is learned behavior that is dependent on appropriate early experiences has been proposed but never fully tested. In the present study this hypothesis was indirectly tested in 73 captive adult chimpanzees (Pan troglodytes; 27 wild-born and 46 captive-born). Bed-building and use were tested experimentally by the introduction of three sets of bedding materials. Over 200 hr of scan-sampling data were collected during 45-min observations following introduction of the bedding material. The wild-born subjects built and used beds significantly more often than the captive-born subjects. Also, wild-born subjects used more complex techniques during construction. Captive-born subjects that were mother-reared through early adolescence spent more time building and using beds than their nursery-reared counterparts. These differences remained consistent even when previous adult experience with bedding (measured as naturalistic vs. traditional housing) was accounted for. These results suggest that bed-building is a learned behavior that requires early experience and practice for acquisition.     

Social development in nursery-reared pigtailed macaques (Macaca nemestrina)

The social development of 240 nursery-reared pigtailed macaques (Macaca nemestrina) was studied from postnatal weeks 4 to 32. The objectives of the study were to document developmental trends and evaluate social behavior in laboratory-reared M. nemestrina raised at the University of Washington Infant Primate Laboratory, and to identify husbandry factors that might affect early social development. Only infants who had not undergone invasive postnatal experimental manipulation and had no chronic illness or injuries were included in the study. Infants were separated from their mothers and housed singly, but had access to peers for 30 min a day, 5 days a week, in a large playroom. Play and social behaviors emerged early in development, increased during the developmental period studied and occupied a large portion of the infants' time budgets. Although disturbance behaviors occurred with some frequency and duration early in development, they occupied a very small portion of the infants' time budget at 8 months of age. Weaning from infant formula at 16–19 weeks retarded development of play behavior. Permanent removal of a cloth comforter (diaper) during weeks 20–24 had no long-term behavioral effects. It was concluded that at 8 months of age these infants showed relatively normal species-typical behavioral repertoires. Am J Primatol 41:23–35, 1997. © 1997 Wiley-Liss, Inc.     

Development of visual preference for closely related species by infant and juvenile macaques with restricted social experience

Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.     

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.     

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.     

Nonsocial behavior of captive infant gorillas

Frequencies of eight nonsocial behaviors (object contact, environmental exploration, mouthing, self-directed behavior, display behavior, solitary behavior, rest, and locomotion) were obtained for 20 infant lowland gorillas (Gorilla gorilla gorilla) between 14 and 36 months of age. They lived in 13 groups in 10 zoological collections. Approximately 12 hours of one-zero data were collected on each animal. Behavioral data were analyzed with regard to the following independent variables: rearing history of the focal animal (mother-reared vs. human-reared), time of day (a.m. vs. p.m.), sex of the focal animal, age of the focal animal, and complexity of the physical and social environment. Results indicated significant differences in the frequency of behaviors within each independent variable, including selfdirected behavior, rest, environmental exploration, and display behavior with rearing history. Additional significant differences in the frequencies of behavior were also found, including mouthing behavior and locomotion with infant age.