Uprooted trees facilitate the psychological well-being of captive chimpanzees

After the introduction of uprooted trees to their environment, the behavior of 28 socially housed, laboratory chimpanzees (Pan troglodytes) was studied for five months. Subjects used the tree during 41.9% of the data points collected during the first day trees were introduced. Thereafter, the mean for tree use dropped to 3.5% and remained fairly consistent. Immature subjects used the trees significantly more than did adult subjects, as measured by the Mann-Whitney U-test. No sex difference was detected. The trees elicited a variety of species-appropriate behaviors. Increasing the similarity between the behavior of captive and wild chimpanzees can be viewed as promoting the psychological well-being of the captive animals.     

Observations of increased activity and tool use in captive rhesus monkeys exposed to troughs of water

This study investigated the effects of water troughs on nonhuman primates housed in a captive environment. Two groups of rhesus monkeys (Macaca mulatta) were exposed to water-filled troughs under three conditions: (1) standing water, (2) running water, and (3) a replication of standing and running water with novel objects. The effects of water exposure were assessed using a pretest phase (baseline), test phase (trough present), and posttest phase (baseline) design for each of the three conditions. Standing water produced different effects from running water. Monkeys were more active in the presence of standing water (higher levels of exploration and lower levels of social contact and grooming) than during baseline observations. In contrast, they were significantly more passive during the running water condition (higher levels of social contact) than baseline. Neither physical condition nor responses to dominance testing varied systematically over phases or between conditions. Tool use was observed during the standing water phases of Conditions 1 and 3. Three females from one group used a variety of cup-like containers as drinking utensils. A larger number of animals used the trough to soak chow prior to ingestion, and virtually all of the animals used the trough as a drinking source. These results suggest that exposure to water sources may elicit a broad spectrum of species-typical activity and may be a simple and inexpensive way to enrich the environment of captive rhesus monkeys. © 1993 Wiley-Liss, Inc.     

Control of postpartum mating behavior in free-ranging rhesus monkeys

This paper explores the effect that a dependent rhesus macaque infant (Macaca mulatta) has on the timing of its mother's resumption of mating. Toward this end, behavioral data from the rhesus populations at Tughlaqabad, India, and Cayo Santiago, Puerto Rico, are compared. Specifically, the intervals between parturition and subsequent resumption of mating for individual parous females are examined in order to shed light on the relative importance of environmental and internal factors (such as lactational infertility) in the control of rhesus mating behvior. At both study sites it was found that the later a given female gave birth during a birth season the shorter was her parturition-mating interval and the younger was her infant when she resumed mating activity. It is suggested that this finding is the result of an interaction of environmental and internal factors; both act in concert to determine how soon after parturition a particular rhesus female will resume mating activity.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Increased cage size does not alter heart rate or behavior in female rhesus monkeys

Newly proposed federal regulations will mandate that singly caged non-human primates be kept in cages larger than the current minimum standard, or be given 4 hours in an exercise cage per week. In order to evaluate the effectiveness of increasing cage size in improving well-being, the behavioral and heart rate responses of 10 female rhesus monkeys (Macaca mulatta) to three different cage sizes were measured. With the exception of vocalizations, no significant differences in behavior were obtained. Grunts increased in the largest cage, following the birth of an infant in a cage within view of the test cages. No differences with respect to cage size were found in heart rate or activity level, although there were significant variations at different times of day. We conclude that modest increases in cage size are less likely to enrich the environment of singly caged laboratory primates than are changes in social opportunities or increases in environmental complexity.     

Influence of food distribution on behavior in captive bongos,Taurotragus euryceros: An experimental investigation

A feeding experiment was conducted to test if Bongo antelopes, being selective feeders searching for clumped quality food, show similar behavior changes as primates under similar conditions. One group of 3 females and 3 calves of Dvur Kralove Zoo was either fed clumped (all food, i.e., leaves and branches of 4 species of tree plus rye grass in one heap), or the same amount distributed over as many heaps as animals present. No increase in agonistic interactions under clumped conditions was found, but non-agonistic and sociopositive patterns increased significantly. Intake of low quality food increased under clumped conditions. Social distances and enclosure use were not significantly different. These findings are in accordance with predictions from models developed for primate feeding strategies, and suggest that selectively feeding antelopes possess behavioral mechanisms for tension-reduction similar to “contest-type” primates. Zoo Biol 16:237–245, 1997. © 1997 Wiley-Liss, Inc.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

The social grooming of captive female rhesus monkeys: Effects of the births of their infants

We observed the grooming interactions of 13 female rhesus monkeys (Macaca mulatta)before and for 12 weeks after the births of their infants. Mothers groomed for similar amounts of time before and after the birth of their infants, but after the birth, the grooming they directed to their infants may have been at the expense of that directed to other partners. Lactating females did not receive more grooming from other females but were approached more often, suggesting that they were more attractive. Mothers that groomed their infants most groomed others least, as if grooming time was limited for each mother or as if she was trying to compensate for avoiding interactions with other partners. Mothers of male infants groomed others more than mothers with female infants did, which might be due to mothers with daughters receiving more aggression and therefore avoiding interaction. Experienced and high-ranking mothers groomed their newborn infants considerably more than primiparous mothers did in the 24 hr following birth. Grooming was preferentially directed at close kin before the births of the infants. Mothers tended to groom higher-ranked partners more than they were groomed by them, and they tended to receive more grooming from lower-ranked partners than they gave, as suggested in models of rank attractiveness.     

Factors affecting social behavior and reproductive success of male rhesus monkeys

This paper reviews aspects of life history that influence the reproductive success of male rhesus monkeys. Recent theories propose that there is some optimum level of inbreeding for each population and that behaviors related to group transfer by males are the result of selection pressure toward such an optimum. Group changing by males is clearly linked to the effects of testosterone at sexual maturation. A male’s maternal genealogical rank is not consistently related to the age at which it leaves the natal group, but social interactions within the natal group may influence the age of departure. Choice of the new group is influenced by the operational sex ratio and the presence of maternal relatives. Rank in the new group is positively correlated with seniority. Seniority, in turn, is influenced by the rank of the male’s natal group, his mother’s genealogical rank, and the presence of male siblings in the new group. Much of this effect is due to the high mortality of males born to females and/or groups of low rank. Most studies show a positive association between male reproductive success and rank. Males from high-ranking groups and/or maternal genealogies that join groups containing brothers tend to remain in those groups longer, attain a higher rank, and probably achieve higher levels of reproduction than other males.     

Seasonal changes in reproductive behavior in two ovariectomized female rhesus monkeys treated year-round with estradiol

Two ovariectomized female rhesus monkeys treated year-round with estradiol-filled capsules were used in hour-long behavioral tests with male rhesus monkeys both in and out of the normal breeding season. The study was designed primarily to test male hormonal responses to copulatory behavior and it was expected that behavior of the females would be essentially the same under both seasonal conditions. Several behaviors of the female, however, were found to fluctuate on a seasonal basis, namely (1) proximity to the male, (2) grooming of the male, (3) sexual presentations, and (4) threatening away (a form of sexual invitation). All of these behaviors, except proximity, were found to be positively correlated with the male partner's testosterone levels before and after the behavior test in the only test condition in which most males ejaculated. The preliminary suggestion is made that these females responded to some cue, either from the environment or from the males, that caused a change in their behavior between breeding and nonbreeding seasons despite the constant hormonal environment provided by the estradiol capsules. Since the same behaviors which were sensitive to seasonal effects were positively correlated with male testosterone levels, it is possible that the male's hormonal status affects affects female behavior.     

A test of the generalizability of the interval scale developed for social behavior of rhesus monkeys

An interval scale of behavior would be useful in the study of social relations because it would allow the whole behavioral repertory to be used simultaneously and would allow greater flexibility in statistical manipulation. Maxim has developed such a scale using isolated dyads of unfamiliar monkeys. The typical social environment of monkeys, however, consists of familiar monkeys in mixed age and sex groups. This study replicates Maxim's procedure and tests the applicability of a scale developed with isolated dyads to groups of familiar monkeys. The scale developed here differed substantially from Maxim's. Behavior of monkeys in these groups was much more variable than behavior of monkeys in Maxim's isolated dyads. Behaviors at the extremes of the scale were similarly arranged in both scales, but behaviors in the central region were more labile and disordered. Distances between behaviors at the extreme of this scale were significantly larger than those in the central region whereas there were no differences in Maxim's scale. While some of these differences may be accounted for by group size and familiarity, several difficulties remain. Some behaviors may change meaning across different contexts and social relationships. The generalizability of these scales, therefore, may be limited to the behavior of groups of similar composition and familiarity.     

Social enrichment of the environment with infants for singly caged adult rhesus monkeys

The practicability of social enrichment for singly caged adult rhesus monkeys was examined. Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults. An adult-infant pair was considered compatible when (1) the two animals started huddling with each other within the first 5 days after pair formation and (2) the infant showed no signs of depression and took its share from a limited amount of favored food. Adult-infant pairs were compatible in 90% (26/29) of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant. There was no evidence that partners lost interest in each other during 7–11 months of follow-up observations. Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they had lived with their young companions for 4 months. It was concluded that the often-heard notion that rhesus monkeys are highly aggressive should not prevent simple attempts to provide singly caged animals with a companion.     

Seasonal breeding in rhesus monkeys: Influence of the behavioral environment

The accepted model of breeding seasonality in rhesus monkeys states that females become reproductively active in response to an environmental cue and that males become sexually active in response to ovulating females. This model must be modified to include direct responses of the male to the physical environment, endocrine responses of males to sexual activity, and responses of the female to the sexual activation of fellow group members. The complex set of social stimuli that influences the breeding readiness of both sexes may serve to delimit more precisely the annual periods of conception and birth than would be the case if each individual responded only to the changing physical environment.     

Partner effects on food consumption in brown capuchin monkeys

It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption.     

Laboratory assessment of temperament and environmental enrichment in rhesus monkey infants (Macaca mulatta)

This study investigated the combined effects of early temperamental characteristics and environmental enrichment on a variety of developmental measures in nursery-reared rhesus monkey infants. Twenty-three infants, reared in either standard laboratory cages or enriched environments, were tested during the 1st month of life for interactive, motor, and temperamental capabilities and characteristics. At 8 months of age, all subjects were assessed on a second series of tests designed to measure their problem-solving skills, motor capabilities, and temperamental responses under challenge. Results indicated that enrichment was associated with higher scores on subsequent problem-solving and motor tests. However, such effects were found to combine with early temperament ratings. Specifically, individuals performing best on the 8-month tests had not only been reared in enriched environments, but also had been rated low on fearfulness during the early assessment. In addition, individuals scoring poorest had been rated as fearful initially in addition to being reared without enrichment. Results indicated that while high ratings on early laboratory assessments of fearfulness may be predictive of poorer problem-solving performance under challenging conditions, these adverse effects may be partially attenuated by environmental enrichment.     

Sociosexual behavior of captive sichuan golden monkeys (Rhinopithecus roxellana)

The Sichuan golden snub-nosed monkey, Rhinopithecus roxellana, is an endangered Colobine endemic to China. The social and reproductive behavior of this species are little known, and it has rarely been kept in captivity outside China. Results from observations of a captive golden monkey pair revealed some unusual details of sociosexual behavior. Both members of the pair mounted one other, and female mounting of the male occurred nearly as often as the reverse. Male mounts were always preceded by a stereotyped behavioral sequence that included distinct facial and vocal displays. Female mounts occurred in response to male solicitation (presenting). No evidence of ejaculation was observed in association with mounts, although mounts were only observed in a distinctly sexual context. Sexual behavior was associated with aggressive displays by one or both animals and with apparently proceptive behavior by the female. All sexual behaviors showed a peak near the end of the study, although the female was continually receptive throughout the 2-month study period.     

Atretogenic action of estrogen in rhesus monkeys: Effects of repeated treatment

The effects of 17β-estradiol (E₂), administered in Silastic capsules for 24 hours at intervals of 10 or 14 days, on follicular development and menstrual cycle characteristics were studied in 13 rhesus monkeys. In seven monkeys receiving E₂ at l0-day intervals for 50 treatment periods, new follicles frequently developed between treatments but usually regressed. In seven instances, the follicles persisted longer than expected but were steroidogenically suppressed and regressed spontaneously. Ovulation occurred in only two instances. In six monkeys receiving E₂ at 14-day intervals, new follicles developed regularly, with seven ovulations occurring in 37 treatment periods. A persistent anovulatory follicle was noted in only one instance. Menstruation occurred with equal frequency, and the interval from treatment to onset of menstruation was not significantly different regardless of treatment or the occurrence of ovulation; the intervals between menstruation approximated those of normal menstrual cycles. In general, following termination of treatment, menstrual cycles returned to normal quickly. These data indicate that E₂ administered intermittently at 10-day intervals effectively suppresses ovulation, and they provide new insight into the actions of E₂ on folliculogenesis in primates.     

Birth sex ratios and maternal social rank in a captive colony of rhesus monkeys (Macaca mulatta)

Data from a 35-year study of rhesus macaques (Macaca mulatta) at Madingley, Cambridge, were used to investigate sex ratio biases associated with maternal rank. Data were available from two colonies, the Old colony (1960–81) and New colony (1982–93). Overall, top-ranking mothers gave birth to 30.9% sons, while non-top mothers gave birth to 58.4% sons. Among non-top mothers, middle- and bottom-ranking ones had 59.0 and 55.0% sons, respectively. Top mothers' daughter biases were strongest in matrilines with two adult females in the year the infants were conceived (15.4 sons and 14.3% sons in Old and New colonies). Non-top mothers' son biases (88.9 and 71.0% in Old and New colonies) were strongest in matrilines with 3 females. The findings are discussed in relation to the colonies' small matriline sizes and data on breeding performance and infant survival, which indicate the costs to mothers of different rank of having different sex infants. Overall, top-ranking mothers were more likely to breed in two successive years (78.6%) than non-top mothers (56.7%). Infant survival to 7 days was significantly higher in the New colony (89.0%) than the Old colony (75.3%), with daughters born to Old colony mothers doing especially poorly. We point out that between-group and between-species comparisons of sex ratio effects depend critically on how females are assigned to rank categories, and require information about divergences of sex ratios from 50:50 in each category. © 1996 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.