Influence of kinship and spatial density on reconciliation and grooming in rhesus monkeys

Some cercopithecine primates direct disproportionate amounts of grooming, huddling, and agonistic support toward maternal kin. Disproportionate amounts of aggression are also directed toward maternal kin, however, suggesting that mechanisms that restore relationships damaged by aggression, such as reconciliation, might be biased toward these preferred social partners. Studies investigating kinship effects and reconciliation are inconsistent, however, perhaps because of differences in the environmental conditions under which behavior was observed. In order to test the effects of kinship and spatial density on affiliative and reconciliation behavior, we conducted focal and scan sampling on a group of rhesus monkeys (Macaca mulatta) living in an outdoor corral under low spatial density conditions. We then compared this data to previously published data on a group of the same species living under higher spatial density conditions. Neither overall grooming nor reconciliation were affected by spatial density once correction procedures were applied. Grooming was kin biased at both study sites, whereas reconciliation was kin biased only in the low-density group. Although data failed to support a Coping Model according to which grooming and reconciliation should go up under higher densities, we suggest that coping may be reflected not so much in overall rates of behavior but in strategic partner choices, such as the increased importance monkeys under crowded conditions appear to attach to nonkin partners. © 1996 Wiley-Liss, Inc.     

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.     

Reciprocity in play,grooming, and proximity in sibling and nonsibling young rhesus monkeys

Play, grooming, and proximity, and the degree to which these were reciprocated between pairs, were studied in immature sibling and nonsibling rhesus monkeys (Macaca mulatta)in four established captive groups over two seasons. “Interaction reciprocity” and “partner reciprocity” were assessed for each dyad for each of the three behaviors. In play, interaction reciprocity was based on the ratio between the play initiations by each dyad member,in grooming on the ratio between the grooming durations by each dyad member, and in proximity on the relative responsibility for proximity maintenance. Two or three most frequent (top) partners for each behavior were found for each individual. If two monkeys were among each other’s top partners, they were said to be reciprocal partners. Monkeys played with nonsiblings as much as with siblings but spent more time grooming and in proximity with siblings than with nonsiblings. Same-age nonsiblings (peers) were more frequent partners than other nonsiblings for each behavior. Siblings’ grooming interactions were more reciprocal than those of nonsiblings. There was no such effect for play and proximity. All-male dyads tended to be more reciprocal in play interactions, and all-female dyads tended to be more reciprocal in grooming interactions. In play, but not in grooming or proximity, the interaction reciprocity of reciprocal partners was higher than that of nonreciprocal dyads. It is argued that the three behaviors have similar roles in infant’s social development but they differ in the expression of this role. Hence the reciprocity patterns vary with the behavior.     

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.     

The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

CBC and serum chemistry differences between Indian-derived and Chinese–Indian hybrid rhesus monkey infants

Hematological and clinical biochemistry measures are commonly utilized as indicators of the health status of nonhuman primates. Among individuals in a population of a given species, there may be considerable variation in these parameters. Still wider variation may be found among different strains or subspecies of some orders. To date, few studies have addressed this phenomenon among strains of nonhuman primates of a given species. Blood samples for hematological and serum biochemical analyses were obtained from 29 Indian-derived and 13 Chinese-Indian hybrid nursery-reared rhesus macaque infants. Total protein, mean corpuscular hemoglobin concentration, mean corpuscular hemoglobin, erythrocyte count, hemoglobin, and hematocrit were all higher in the hybrid infants. These results indicate that the origin or strain of the animal should be considered when designing studies using rhesus macaques. © 1996 Wiley-Liss, Inc.     

Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees

Handclasp grooming is a unique social custom, known to occur regularly among some, but not all populations of chimpanzees (Pan troglodytes). As with other cultural behaviors, it is assumed that this distinctive grooming posture is learned socially by one individual from another. However, statistical comparisons among factors thought to influence how a behavior spreads within a group have never, to our knowledge, been conducted. In the present study, the origination and spread of handclasp grooming in a group of captive chimpanzees was followed throughout more than 1,500 h of observation over a period of 12 years. We report on the frequency, bout duration, and number and demography of performers throughout the study period, and compare these findings to those reported for wild populations. We predicted that dyads with strong affiliative ties, measured by time spent in proximity to and grooming one another, were likely to develop a handclasp grooming partnership during the study period. A quadratic assignment procedure was used to compare correlations among observed frequencies of grooming and proximity with handclasp grooming in all possible dyads within the group. As predicted, the formation of new handclasp grooming dyads was positively correlated with the rate of overall grooming and proximity within a dyad. In addition, in nearly all dyads formed, at least one individual had been previously observed to handclasp groom. We concluded that affiliation and individual experience determines the transmission of handclasp grooming among captive chimpanzees.     

Reciprocity and partner preference in grooming of female blue monkeys

Grooming among adult and older juvenile females in a wild group of blue monkeys (Cercopithecus mitis stuhlmanni) is analyzed and related to agonistic behavior. Both grooming and agonistic behavior were less frequent than would be expected in baboon and macaque groups. Fair shares of grooming were given and taken, both within and between interactions, in amost dyads, and all females were seen to groom with at least half the others. The reciprovity of grooming was its most outstanding feature. There was no evidence that grooming was preferentially directed at kin. Frequent grooming partnerships fell into two clusters, one of which ranked higher than the other. We suggest that grooming throughout the group helps to establish a coherent team of females which effectively, defends its territory in daily encounters at the boundaries with neighboring groups.     

The human Duffy blood group in rhesus monkeys1

There is good evidence that susceptibility to Plasmodium vivax infection and to P. knowlesi erythrocyte invasion is influenced by certain human Duffy (Fy) blood group antigens. Since P. knowlesi readily infects rhesus monkeys (Macaca mulatto), it was not surprising to find an Fy-like antigen on rhesus erythrocytes. Using human Fy antisera in elution and absorption experiments, we found that all 40 rhesus monkeys tested displayed the Fy(a-b +) phenotype. Furthermore, the rhesus Fy^bantigen was inactivated by chymotrypsin but not by trypsin, suggesting that it is homologous to the human Fy^bantigen. Preliminary serological analyses and enzyme hydrolysis experiments suggest that none of the 13 blood group systems that we have described in rhesus are analogous to the human Fy system. Thus, it appears that there is no Duffy-like polymorphism in rhesus monkeys.     

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.     

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.     

Assessment of motor function of the hand in aged rhesus monkeys

In the elderly, intact motor functions of the upper extremity are critical for the completion of activities of daily living. Many studies have provided insight into age-related changes in motor function. However, the precise nature and extent of motor impairments of the upper extremity remains unclear. In the current study we have modified two tasks to assess hand/digit function in both young and aged rhesus monkeys. We tested monkeys from 9 to 26 years of age on these tasks to determine the level of fine motor performance across the adult age range. Compared to young monkeys (9–12 years of age), aged monkeys (15–26 years of age) were mildly impaired on fine motor control of the digits. These findings are consistent with previous studies that have found age-related impairment in fine motor function. However, the magnitude and extent of impairment in the current study does differ from previous findings and is likely due to methodological differences in the degree of task complexity.     

Effects of woodchips and buried food on behavior patterns and psychological well-being of captive rhesus monkeys

The effects of adding woodchip litter to bare-floored pens, burying monkey chow in the woodchips, and scattering sunflower seeds in woodchips was studied in 2 stable social groups of rhesus macaques (Macaca mulatta) to ascertain the effects of these manipulations on levels of foraging, exploration, abnormal behavior, social interactions, and urinary cortisol levels. The addition of woodchips increased exploration and feeding levels and decreased social interactions. Burial of regular monkey chow in woodchips had little effect on behavior beyond that of the woodchips alone, increasing exploration and decreasing passivity. The addition of sunflower seeds to the woodchips encouraged increased feeding and exploration and led to decreases in passivity and social interaction. There was little discernible effect of woodchip enrichment on urinary cortisol values. In contrast to some previous studies, there was no effect of wood chips or sunflower seeds on the occurrence of agonistic interactions, play, or abnormal behavior patterns.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

Effect of testosterone on epididymal proteins in castrated rhesus monkeys

The effect of testosterone on regulation of epididymal protein synthesis has been investigated in castrated rhesus monkeys (Macaca mulatta). The proteins in the treated monkeys were characterized using polyacrylamide gel electrophoresis (under nondenaturing and denaturing conditions) and electrofocusing. At least four distinct proteins have been shown to be synthesized by the monkey epididymis under testosterone influence. Two of these proteins were detected following two days of testosterone treatment while the other two proteins were detected after a six-day treatment period. None of these proteins was detectable in monkeys treated with estradiol for six days. Electrofocusing of epididymal cytosol proteins from untreated and testosterone-treated and castrated monkeys also confirmed the presence of four androgen-dependent proteins in this species. The isoelectric points of these proteins were shown to range between 5.8 and 6.4. The molecular weights of these proteins were found to vary between 47,500 and 66,000. The in vitro incorporation of ³H-labeled amino acids was markedly greater in the androgen-primed epididymis as compared with the control tissue.     

Immunogenetic studies of rhesus monkeys. 6. Absence of the human Xga blood group on rhesus erythrocytes1

It was not possible to demonstrate Xg^a on the erythrocytes of any of 140 rhesus monkeys of both sexes tested with human antiserum rendered specific for Xg^a by absorption.     

The association between rank and reproductive success of male rhesus monkeys

The paternity of 202 of 220 offspring of rhesus monkeys housed in six separate half-acre field cages at the California Primate Research Center was determined by genetic marker techniques. Reproductive success of the adult males was statistically significantly correlated (r = 0.76, P <0.0005) with rank. Marked systematic changes in reproductive success were, however, observed for two adult males during the three years covered by this study. Based upon these results and those of another study, it is argued that changes in rank position typically follow, rather than precede, changes in reproductive success.     

Maternal rejection and infant play in rhesus monkey infants

In five-minute records in which they were rejected by their mothers, passive preventions of nipple access, 11- to 15-week-old group-living rhesus monkey infants (Macaca mulatta) initiated fewer playful conctacts with others relative to the other kinds of social contact they initiated, while their overall rates of initiating social contacts may not have been reduced. Whether acts of maternal rejection are costly and distressing to the infant may depend on the nature of the social companions available for it and until more is known of the context of such acts, hypothesis about weaning conflict will be difficult to test in detail.