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.     

Physiology of maternal separation in a bonnet macaque infant

A bonnet monkey infant (M. radiata) was monitored both physiologically and behaviorally during a separation experiment in which both its mother and other conspecifiecs were removed from its social group leaving the bonnet infant with three adult pigtailed females. The separated infant exhibited the characteristic slouched posture of depression and physiological changes including decreases in the heart rate and body temperature, increases in cardiac arrhythmias, and alterations in sleep patterns, as has been previously described in separated pigtailed infants. Persistent decreases in heart rate and body temperature were noted following reunion with the mother, possibly reflecting a disturbance in the mother-infant relationship secondary to the mother's having come into estrus during the period of separation. This study indicates that the physiological correlates of maternal separation previously described in pigtailed infants are not species specific.     

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.     

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.     

Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)

The developmental origin of abnormal behaviors is generally associated with early rearing environments that lack sufficient physical and sensory stimulation. However, other factors should also be considered. A large sample of captive chimpanzees (128 males and 140 females) was surveyed for the presence or absence of 18 abnormal behaviors. Origin variables included the subject's source (zoo, pet, performer, or laboratory), rearing (mother‐ or hand‐reared), and sex. Animals were assessed while held at the Primate Foundation of Arizona, University of Texas M. D. Anderson Cancer Center, or White Sands Research Center. There was a confound among origin variables; more hand‐reared animals than expected were from laboratories. Logistic regression tested the relationship of rearing and source, with sex as a secondary predictor variable, to each of the abnormal behaviors. There was no clear association between any abnormal behavior and source. However, for coprophagy, relative to animals from the laboratory, zoo animals tended to show a higher prevalence, while performers tended to show a lower prevalence (when rearing and sex were controlled). Rocking and self‐sucking were significantly more likely in hand‐reared animals. Coprophagy and depilation of self were significantly more likely in mother‐reared animals. When rearing and source were statistically controlled, the only significant sex difference was a higher prevalence of coprophagy in females and a higher prevalence of rocking in males. In a second, smaller sample of 25 males and 33 females from Southwest Foundation for Biomedical Research, no significant sex association was found for coprophagy, urophagy, rocking, or self‐depilation. In this second sample, coprophagy was also significantly more likely in mother‐reared than hand‐reared subjects. The association of some abnormal behaviors with mother‐rearing suggests that some form of social learning may be involved in the origin of some of these behavior patterns. This indicates that some abnormal behaviors may not be always be indicative of reduced psychological well‐being in captive chimpanzees. Am. J. Primatol. 48:15–29, 1999. © 1999 Wiley‐Liss, Inc.     

Effect of solar eclipse on the behavior of a captive group of chimpanzees (Pan troglodytes)

A captive group of chimpanzees, housed in an outdoor compound at the Yerkes Regional Primate Research Center, was observed during the annular solar eclipse of May 30, 1984. The behavior of each animal was recorded using an instantaneous scan-sampling technique (Altmann: Behaviour 49:227–265, 1974). Beginning 2 days prior to the eclipse and continuing through the day following the eclipse, data were collected from 1100 to 1300 hours daily. At 1214 hours on the day of the eclipse, when the sky began to darken and the temperature began to decrease, solitary females and females with infants moved to the top of a climbing structure. As the eclipse progressed, additional chimpanzees began to congregate on the climbing structure and to orient their bodies in the direction of the sun and moon. At 1223 hours, during the period of maximum eclipse, the animals continued to orient their bodies toward the sun and moon and to turn their faces upward. One juvenile stood upright and gestured in the direction of the sun and moon. Sunlight began to increase at 1225 hours, and as it became brighter, the animals began to descend from the climbing structure. The behaviors exhibited by the group during the period of maximum eclipse were not observed prior to or following the eclipse nor as darkness approached at normal, daily sunset. These data indicate that a solar eclipse, a rare and uncommon environmental event, can influence and modulate the behavior of chimpanzees.     

Mother–calf interactions and social behavior development in Commerson’s dolphins (Cephalorhynchus commersonii)

Mother–calf interactions and the behaviors of mothers during separation from their calves were examined in four Commerson’s dolphin (Cephalorhynchus commersonii) mother–calf pairs. Four infants were observed: 56.8 h over 30 days from birth to 263 days of age, 36.9 h over 20 days from birth to 149 days of age, 10.4 h over 3 days from birth to 2 days of age, and 15.0 h over 3 days from birth to 2 days of age. All four pairs shared common characteristics in the rate and frequencies of mother–calf interactions and the behaviors of mothers during the first week of life. After the first week, individual differences in changes in the frequency of each behavior were observed. The three behaviors considered representative of maternal care (parallel swimming, synchronous breathing, and body-to-body contact) were frequently performed in the first week; thereafter, the frequencies declined. Separate behaviors of mothers were infrequent during the first week and increased with an increase in infants’ age. Bumping by infants increased with time, suggesting an increase in soliciting by calves and conflict between mothers and calves. The frequency of flipper-to-body rubbing also changed but in a complex manner, probably because the calves needed to learn how to perform this behavior from their mothers and because initiator and recipient of this behavior can be changed quickly.     

The effect of peer contact upon physiological response to maternal separation

The response of both human and nonhuman primate infants to separation from their mothers is characterized by agitation or protest behaviors followed by a behavioral depressive reaction. In monkeys, this behavioral syndrome has striking physiological correlates, including heart rate and sleep disturbances. There is, however, considerable individual variability in response to maternal separation. The authors hypothesized that the amount of contact with particular, familiar conspecifics might account for some of this variability. In support of this notion, data are presented that indicate that pigtailed monkey infants who have been separated from their mothers but who maintain relatively high levels of peer contact do not show as severe decreases in heart rate during maternal separation as do those that exhibit less peer contact.     

Factors determining tool-using ability in two captive chimpanzee (Pan troglodytes) colonies

The influence of several determinants of performance in a reaching tool task were studied: rearing history, object experience, and gender. Forty-five chimpanzees between the ages of 7 and 36 years served as subjects. They were chosen from two facilities, each group having different levels of tool experience. Each group was made up of individuals from three rearing conditions: wild born, captive mother reared, and captive nursery reared. Results indicated that wild-born subjects were better at the task than were both groups of captive-born subjects, who performed similarly. Previous experience with reaching tools was not a significant factor in the determination of tool-using ability. Gender differences were not apparent for either group, and the range of ages of chimpanzees tested was not related to tool-using ability.     

Neonatal interactions in pig-tailed macque (M. nemestrina) dyads: Influence on rearing success,infant weight change and behavioral response to reunion with mother

This research assessed the significance of variation in dyadic neonatal interaction for subsequent infant development in pig-tailed macaques. Adult females were selected which differed in parity and reproductive risk. The 29 dyads were housed individually to reduce external environmental influences. Large variation was observed in maternal and neonatal behavior, but it was not significantly associated with maternal or infant risk variables and could not identify six unsuccessfully reared pairs. Among the 23 successfully reared dyads, variation in nutritional and behavioral measures hypothesized to be associated with infant growth were found to be independent of neonatal weight gain. These 23 infants were separated from their mothers after 30 days and their responses at reunion were observed. Some infants clung to the mother's ventrum (attached response) while others jumped away quickly (aloof response). Prior dyadic interactions were not significantly associated with this dichotomous response, nor were maternal and most infant variables. These results suggest that dyads at risk for neonate separation when living in captive groups are not necessarily at risk in individual housing conditions. Further, pig-tailed neonates appear unaffected by variations in mother-infant interactions that do not result in separation, but neonatal characteristics may show continuity across development.     

Le comportement du Chevrotain africain,Hyemoschus aquaticus Ogilby (Artiodactyla,Ruminantia)

The purpose of this study was to test the influence of social isolation during infancy on learning behavior in rats. Rats, reared isolated (n = 55) or paired (n = 60) for a period of 50 days following weaning, were tested on different learning tasks in an operant conditioning chamber. Isolation rearing produced significantly better learning when the training period directly followed the different housing conditions. After a 28 day period of social isolation for the subjects raised paired during infancy no differences in learning between isolated and paired reared animals could be observed. The differences are discussed in relation to the effects of stimulus deprivation.     

Effects of infant-infant separation of young monkeys in a free-ranging natural environment

Five infant rhesus monkeys reared togather in free-ranging natural environment for about eight months were subjected to peer separation. Separation of an infant was inflicted by way of removing all the other infants from their home range. The infants so separated showed exceedingly high levels of locomotion and vocalizations in the beginning of separation phase, but their such excited behaviour did not last for more than a day, and during the remaining separation period they appeared to be quite depressed as mainly indicated by their reduced range of locomotion, reduced motivation for food and water, and reduced level of vocalization and environmental exploration. Thus, the animals showed a biphasic response to separation, which was characterized by an initial phase of ‘protest’ followed by a ‘despair’ stage, basically similar to what has been reported in infant rhesus monkeys subjected to peer or mother separation under laboratory conditions. The main project of which this research was a part is being financed by Indian Council of Social Science Research (ICSSR).     

Procedures for improving maternal behavior in captive chimpanzees

Captive female chimpanzees who have had no opportunity to observe mothers with infants or to interact with infants often show inappropriate maternal behavior, particularly with their first-born infant, and this usually results in the removal of the infant to be human-reared. The present study used two techniques to encourage appropriate maternal behavior in ten pregnant female chimpanzees. These females were housed together with unrelated infant chimpanzees to adopt, or with lactating female chimpanzees and infants to observe. In five cases both techniques were used, in two cases only the first technique was used, and in three cases only the second technique was used. All ten female chimpanzees showed appropriate maternal behavior when their infants were born, in contrast to a group of eight female chimpanzees who had no such experience whose infants had to be removed for human-rearing. It is suggested that these techniques, or adaptations of them, could be applied to many other captive female chimpanzees with similar results.     

Hematological and serum biochemical effects of nursing on the mother in cynomolgus monkeys (Macaca fascicularis)]

The effects of nursing on maternal hematological and serum biochemical values were analyzed in cynomolgus monkeys reared in indoor cages at Tsukuba Primate Center. In our breeding system, infants are usually separated from their mothers at the age of 121 to 180 days. Mother monkeys of such infants were studied hematologically and biochemically (Group B), as were mother monkeys who happened to have nursed their infants past 181 days after parturition (Group A). During the period with their infants, mother monkeys in the latter group showed lower white blood cell counts (WBC) and higher red blood cell counts (RBC), hematocrit values (Ht) and blood urea nitrogen concentrations (BUN) than the mother monkeys who had been separated from their infants. Also, serum calcium concentrations (Ca) were decreased with prolonged nursing periods, indicating that lactation by the mother monkey probably continues even for a period from 181 days to about one year after parturition if she nurses her infant. Lactation during this period may accelerate hematogenesis and protein metabolism in the mother monkey.     

Techniques for hand-rearing tree-shrews (Tupaia belangeri) from birth

In captivity, Tupaia belangeri (Thailand tree-shrew) frequently show aberrant patterns of maternal care which result in the death of offspring. In order to maximize the potential of the tree-shrew as an animal resource for experimental studies we have developed a program for hand-rearing tupaiidae from birth. Newborn tree-shrews were removed from mothers with a history of poor parental care to a nursery maintained under conditions of controlled relative humidity (70 ± 10%) and temperature (25 ± 1°C) on a 12 h dark: 12 h light cycle. The young tree-shrews were fed on a liquid formula until the eyes opened (Day 18–23) and for the subsequent 10 days on a transitional diet until they could feed themselves on solid food. Our hand-rearing protocol appears to conform to the natural weaning pattern of tupaiids. Food consumption during the liquid diet phase was linearly related to age and the increase in body weight in both sexes. The initial growth rate of male and female hand-reared tree-shrews was slower than that of maternally reared animals during the liquid diet phase. The growth rate accelerated subsequently and the body weight of hand-reared tree-shrews eventually reached that of maternally reared animals of the same sex. Various developmental changes occurred during the same period in artificially and naturally reared animals. In both hand-reared and maternally reared groups, the growth rate of male tree-shrews exceeded that of females from about Day 40 onward. The accelerated growth rate of male tree-shrews was in apparent association with an increase in androgen secretion at the onset of puberty. The high fecundity of tree-shrews in captivity reinforced with a program for hand-rearing the young make T belangeri a potential alternative to more conventional laboratory species in specific areas of biomedical research.     

Transfer and Acclimatization Effects on the Behavior of Two Species of African Great Ape (<Emphasis Type="BoldItalic">Pan troglodytes</Emphasis> and <Emphasis Type="BoldItalic">Gorilla gorilla gorilla</Emphasis>) Moved to a Novel and Naturalistic Zoo Environment

Studying the effects of moving animals to new enclosures is of value to both captive managers and to scientists interested in the complex interplay between environment and behavior. Great apes represent some of the greatest challenges in this regard. Given the cognitive sophistication of these species and the substantial investments in new primate facilities, these investigations are particularly important. Using post-occupancy evaluation (POE) methodology, we compared behavior exhibited by chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla) in indoor hardscape-type exhibits to behavior of the same individuals in new naturalistic enclosures with outdoor access. In the new facility, chimpanzees showed decreases in the frequency of abnormal behaviors and visual monitoring of humans (attention behaviors) whereas gorillas exhibited reduced agonism as well as decreased attention behaviors. Both gorillas and chimpanzees demonstrated higher rates of inactivity after transfer to the new facility. All subjects in addition demonstrated transitory changes in behavior after the move to the new facility (higher rates of scratching in yr 1 than in subsequent years), indicating a period of acclimatization. Seasonal effects on feeding behavior and activity levels (both species were more active in the winter) were evident as well. The results indicate that behavioral adjustment to a new facility is an extended process for both species and that seasonal effects should be considered in longitudinal analyses of acclimatization. Behavioral patterns supported the benefits of naturalistic, functional exhibit spaces and the utility of post-occupancy evaluations in assessing captive animal welfare.     

Early social environment interferes with the development of NADPH-diaphorase-reactive neurons in the rodent orbital prefrontal cortex

The influence of early parental deprivation on the development of NADPH-diaphorase-(NO-synthase) reactive neuron numbers in subregions of the orbital prefrontal cortex (ventrolateral orbital, lateral orbital, and agranular insular cortex) was quantitatively investigated in the precocious lagomorph Octodon degus. Forty-five-day-old degus from three groups were compared: (1) repeated parental separation: degus that were repeatedly separated from their parents during the first three postnatal weeks and thereafter raised in undisturbed social conditions; (2) chronic isolation: degus that were raised under undisturbed social conditions until postnatal day 21, and then were reared in chronic social isolation; and (3) control: degus that were reared undisturbed in their families. Compared to the control animals the ventrolateral orbital prefrontal cortex and agranular insular cortex of the two deprived groups displayed significantly decreased density of NADPH-diaphorase-reactive neurons (down to 62% in the ventrolateral orbital prefrontal cortex of males, 70% in the agranular insular cortex, and in the lateral orbital prefrontal cortex 80% in both genders). These results confirm that early changes of social environment interferes with the development of limbic circuits, which might determine normal or pathological behaviors in later life.     

Abnormal behaviors,with a special focus on rocking,and reproductive competence in a large sample of captive chimpanzees (Pan troglodytes)

Chimpanzees (Pan troglodytes) are endangered in the wild and may no longer be imported into the United States. Of those animals presently in captivity, candidates for breeding programs must be identified to insure a self-sustaining captive population. Some have suggested that poor reproductive performance might be linked to the performance of abnormal behaviors. In Study 1, three institutions housing breeding colonies of chimpanzees (86 males, 103 females) surveyed their animals for abnormal behaviors, copulatory performance, and, for females, maternal competence. In neither sex was there a positive association between absence of copulation and the presence of any of 18 forms of abnormal behavior. No one abnormal behavior was positively associated with inadequate maternal performance. Contrary to expectations, in both sexes (significantly for females), copulators exhibited more forms of abnormal behaviors than did noncopulators. In contrast, good mothers did show slightly fewer different forms of abnormal behaviors than did inadequate mothers. No specific combination of abnormal behaviors was associated with lack of copulatory performance in either sex or with inadequacy of maternal behavior. Significant sex differences occurred only in 2 of the 18 abnormal behaviors (coprophagy and self-clinging), both with females showing the higher prevalence. In Study 2, the rate of rocking in 5 male and 14 female chimpanzees at the Primate Foundation of Arizona was found to be relatively high among some reproductively competent subjects. Some rocking had forms and contexts indicative of aggressive displays. We conclude that chimpanzees should not be disregarded as potential breeders or as candidates for resocialization and breeding programs solely because they exhibit abnormal behaviors. Anyone involved in assessing well-being needs to be aware of individual differences among animals in the stimuli that may elicit rocking behavior. If they are strangers, they may elicit display rocking which does not indicate a lack of well-being. © 1992 Wiley-Liss, Inc.     

Social Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees

Humans’ two closest primate living relatives, bonobos and chimpanzees, differ behaviorally, cognitively, and emotionally in several ways despite their general similarities. While bonobos show more affiliative behaviors towards conspecifics, chimpanzees display more overt and severe aggression against conspecifics. From a cognitive standpoint, bonobos perform better in social coordination, gaze-following and food-related cooperation, while chimpanzees excel in tasks requiring extractive foraging skills. We hypothesized that attention and motivation play an important role in shaping the species differences in behavior, cognition, and emotion. Thus, we predicted that bonobos would pay more attention to the other individuals’ face and eyes, as those are related to social affiliation and social coordination, while chimpanzees would pay more attention to the action target objects, as they are related to foraging. Using eye-tracking we examined the bonobos’ and chimpanzees’ spontaneous scanning of pictures that included eyes, mouth, face, genitals, and action target objects of conspecifics. Although bonobos and chimpanzees viewed those elements overall similarly, bonobos viewed the face and eyes longer than chimpanzees, whereas chimpanzees viewed the other elements, the mouth, action target objects and genitals, longer than bonobos. In a discriminant analysis, the individual variation in viewing patterns robustly predicted the species of individuals, thus clearly demonstrating species-specific viewing patterns. We suggest that such attentional and motivational differences between bonobos and chimpanzees could have partly contributed to shaping the species-specific behaviors, cognition, and emotion of these species, even in a relatively short period of evolutionary time.