Immunogenetic studies of rhesus monkeys

To assay for transplacental immunization in rhesus monkeys, sera from 253 postpartum females, 31 virgin females, and 40 males were tested for erythrocyte agglutinins. Nineteen percent of the mothers exhibited antibodies, but less than three percent of the virgin females or males did so. Antibodies were detected in 26 percent of the mothers who bore blood group-incompatible infants, in contrast to only eight percent of the mothers with compatible offspring. Thus, blood group incompatibility may lead to transplacental alloimmunization of the rhesus female. Unlike the situation in humans, hemolytic disease was not observed, even when the erythrocytes of the newborn rhesus were coated with maternal antibodies.     

Maternal Responsiveness Increases during Pregnancy and after Estrogen Treatment in Macaques

Maternal responsiveness in primates has long been considered emancipated from endocrine factors and entirely dependent on experience and cognition. Here we report that group-living pigtail macaque females increased their rate of interaction with infants in the last weeks of pregnancy in correspondence with an increase in plasma levels of estradiol and progesterone. Estrogen treatment increased the rate at which ovariectomized rhesus females interacted with infants. This is the first evidence that steroid hormones influence maternal responsiveness in anthropoid primates. All untreated ovariectomized females and nonpregnant females interacted with infants, indicating that although estrogen can enhance responsiveness to infants, ovarian or pregnancy hormones are not necessary for the expression of infant-directed behavior in female macaques. The findings of this study suggest fundamental similarities, rather than differences, in the endocrine modulation of maternal responsiveness in primates and other mammals.     

Subjective assessment of rhesus monkeys over four successive years

Using behaviourally-defined adjectives and a 7-point scale, observers rated all individuals over a year old in a colony of rhesus monkeys every November for four years. Principal component analyses of the ratings provided a basis for the following scores each year: CONFIDENT, EXCITABLE, and SOCIABLE. Two- and three-year old females had higher EXCITABLE scores than males, and adult males were more CONFIDENT than adult females. At all ages, CONFIDENT scores were stable from year to year, whereas EXCITABLE and SOCIABLE scores were not stable until adulthood. However for primiparous females, only their EXCITABLE scores were stable from the ante-natal to post-natal year. One-year males who had had adverse experience in their first eight months were more EXCITABLE, but no less CONFIDENT or SOCIABLE than control males. Finally, correlations between scores of mothers and their yearlings showed that CONFIDENT mothers had CONFIDENT infants and SOCIABLE mothers had SOCIABLE infants, but EXCITABLE mothers had infants who were not CONFIDENT. Scores of mothers and their 1-year olds were also significantly correlated with some measures of their social behaviour taken when the infants were 8, 16, and 52 weeks old.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.     

Infant-directed behavior of rhesus monkeys during their first pregnancy and parturition

To determine whether pregnancy influences the response of rhesus monkeys towards infants, 11 females were observed during 15-min exposures to a 1- to 15-day-old infant at 1- to 2-week intervals throughout pregnancy. No evidence was found for increasing willingness to contact infants as pregnancy progressed. The parturition of 5 of these females was observed, which included 1 live breech birth. These primiparae all established ventral contact with their infants at birth, though most of them appeared to passively allow the infant to initiate contact while their own attention was directed at licking the birth fluids.     

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Infant kidnapping among group-living rhesus macaques: Why don't mothers rescue their infants?

Observations of infant kidnapping among group-living rhesus macaques and anecdotal evidence in the literature indicate that monkey mothers do not attempt to forcibly retrieve their infants from kidnappers even though kidnapping may have potentially fatal consequences for the infant. Based on the available evidence, the potential risk of injury to the mother and/or the infant in case of precipitated conflict with the kidnapper may conceivably account for the lack of maternal intervention during kidnapping. Although this hypothesis requires further testing, maternal refrainment from intervention seems to be a maladaptive response in cases of long-lasting kidnappings by nonlactating females because the infant's life is at stake and the cost of the loss of an infant is presumably higher than the potential risk of injury in a fight.     

Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques

Lactating female rats without their pups exhibit lower HPA responsiveness to stress than nonlactating females. However, responsiveness to stress is similar when lactating females are tested with their pups and the stressor involves a potential threat to the offspring. This study constitutes the first comparison of stress responsiveness in lactating and nonlactating female nonhuman primates. Subjects were 53 multiparous female free-ranging rhesus macaques. Approximately half of the females were lactating and half were nonpregnant/nonlactating. Blood samples were obtained after capture and after overnight housing in an individual cage. Lactating females were tested with their infants. Lactating females had significantly higher plasma cortisol levels than nonlactating females on both days. Having or not having an infant was also a better predictor of plasma cortisol levels among all females than their age, dominance rank, group of origin, time of day at which the sample was obtained, and time elapsed since beginning of the sampling procedure or since anesthesia. Plasma cortisol levels of lactating females were not significantly correlated with post-partum stage or with the cortisol levels of their infants. Capture, handling, and individual housing in a cage are powerful psychological stressors for free-ranging primates. We suggest that the higher plasma cortisol levels exhibited by lactating females reflect greater responsiveness to stress associated with perception of risks to infants. Hyporesponsiveness to stress may not be a general characteristic of lactation in all mammalian species, but a short-term effect of infant suckling that is most apparent with stressors unrelated to the offspring.     

Sex differences in interest in infants in juvenile rhesus monkeys: relationship to prenatal androgen

Yearling rhesus monkey females interact more with infants than do males. However, the continuity of this sex difference throughout the juvenile period is unknown. Human females display similar sexually differentiated interest in infants, and studies of girls with congenital adrenal hyperplasia suggest that this sex difference may be modulated by prenatal androgen exposure. We investigated infant interest in 1- to 3-year-old juvenile rhesus monkeys. Hormonal influences on this behavior were investigated by treating pregnant females with an androgen-receptor blocker (flutamide), testosterone enanthate, or vehicle, early or late in gestation. Subjects were reared in their well-established natal groups, composed of species-typical matrilineal social structures, including members of all ages. Yearling control females interacted with infants more than did yearling control males. At 2 and 3 years of age, the magnitude of the sex difference in interactions with infants increased markedly, producing effect sizes of more than 2.5 standard deviations. These effects are larger than those reported in humans. Androgen treatment did not affect male or female interactions with infants, but late gestation flutamide masculinized aspects of females' interest in infants. Although early flutamide prevented complete masculinization of male genitalia, this treatment was not accompanied by any alterations in the masculine pattern of infant interest. We found no evidence that the robust juvenile sex difference in frequency of infant interactions results from socialization. However, it was largely unaffected by our hormone manipulations. Whether this reflects characteristics of our specific treatments or is evidence of nonhormonal influences on infant interest remains unanswered.     

Sex Differences in Infant Rhesus Macaque Separation–Rejection Vocalizations and Effects of Prenatal Androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation–rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Neonatal deaths in bonnet monkeys born to dams with rudimentary papillae mammae

Deaths due to dehydration and starvation occurred in the early neonatal period in bonnet monkey (Macaca radiata) infants housed with their dams in an outdoor half-acre corral. Dams were found to have small, rudimentary papillae mammae of insufficient size to permit suckling. Both papillary and breast tissue of affected dams were histologically normal; the nipples differed macroscopically from those of normal females only in size. This abnormality accounted for half of the neonatal mortality experienced in this breeding colony over a 5-year period.     

Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta)

In several primate species, males have been shown to exhibit a surge in circulating testosterone during the early postnatal period. This surge has been postulated to play a role in the development of sex differences in behavior. In this study, the role of postnatal testosterone in infant behavioral development was investigated in socially living rhesus macaques. Seven male infants were treated with a GnRH agonist, avorelin, from the first week of life onwards. Ten female infants were exposed to testosterone by implantation of capsules containing testosterone. The behavioral development of these and control infants was recorded from birth to 6 months of age. The sexually dimorphic patterns of play and mounting were not affected by manipulation of postnatal testosterone in either male or female infants. Similarly, most mother-infant interactions were not affected by the hormonal manipulation of infants. Mothers of testosterone-treated females were found to take more responsibility for moving into and out of arm's reach of their infants than mothers of some other groups of infants; however, this measure did not normally differ between mothers of male and female infants. Manipulation of the postnatal testosterone surge does significantly affect penile growth and development, but does not affect the expression of infant sex differences in behavior nor greatly affect the development of the mother-infant relationship in rhesus macaques.     

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.     

Species differences in the interest shown in infants by juvenile female macaques (Macaca radiata andM. mulatta)

Using a focal animal technique, 16 juvenile female rhesus and bonnet macaques (2–3 years old) were observed with respect to the frequency and duration of their contacts with infants (0–1 year old). Each of these subjects was a member of one of four seminatural groups of macaques housed in 0.5-acre field cages at the California Primate Research Center. Rhesus juvenile females became very interested in infants when the latter were quite young, and maintained that interest throughout the study. When the infants were approximately 3–4 months old, the rhesus juveniles spent, on the average, 3.9 min/hr with those infants. By the time the infants were yearlings, the time spent with infants was approximately 6 min/hr. Relative to the rhesus, the bonnet juveniles showed less interest (about 2.2 min/hr) in young (3- to 4- month-old) infants, although by the time the infants were yearlings, the bonnets spent about 5.6 min/hr with them. Rhesus juveniles preferred sibling over nonsibling infants, but the presence of a sibling was not a necessary requirement for infant-directed behavior. The two bonnet juveniles who had infant siblings showed no preference for the latter. These data were interpreted within the framework of Quiatt’s [(1979) Am. Anthropol. 81: 310–319 conclusions about allomaternal behavior. Specifically, it was argued that, to the extent that there are species differences in maternal behavior, there should also be species differences in allomaternal behavior. The species differences in the maternal styles of rhesus and bonnet macaques provide a basis for an examination of this hypothesis.     

Maternal Infant Monitoring in a Free-ranging Group of Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

In nonhuman primates, females with infants visually monitor their infants from a distance to detect and consequently avoid potential threats to their infants. We recorded maternal visual monitoring of infants (infant monitoring) ages 7–18 wk in a free-ranging, provisioned group of Japanese macaques (Macaca fuscata). The infant monitoring rate declined as a function of infants’ ages in weeks and increased when the infants were beyond their mother’s reach, indicating that infant monitoring reflects the vulnerability of infants. Females with infants increased infant monitoring when their infants were handled by other group members but not when their infants moved alone. This suggests that intragroup threats (harassment/mishandling or kidnapping) have a relatively stronger influence on infant monitoring than external threats (predation or infanticide) under the condition of this study. Infant monitoring of middle-/low-ranking females was more frequent than that of high-ranking females when their infants were handled by other individuals. This may reflect greater intragroup threats to infants of middle-/low-ranking females; however, further study is needed to confirm this. During important activities (feeding or grooming), the infant monitoring rate was lower than that during other activities (resting or self-directed behavior). However, even during important activities, females with infants increased infant monitoring when infants were handled. This indicates that females with infants face a trade-off between infant monitoring and other important activities, and even if females have to reduce the time spent on important activities, they increase infant monitoring when their infants face greater potential intragroup threats.     

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.     

Role of nipple stimulation in the suppression of estrous cyclicity during extended lactation in the rat

The role of nipple stimulation in the suppression of the estrous cycle during extended lactation was studied in rats subjected to either total, partial, or sham excision of the nipples. Each female cohabited with 4 pups, 4-14 days old, over a period of 70 days postpartum, during which vaginal smears were recorded daily. Initially, regardless of the presence of nipples, all rats exhibited a postpartum diestrus that lasted for 12-20 days. Intact females (bearing 6 pairs of nipples) continued to exhibit successive prolonged diestrous phases over 70 days of lactation. A comparable result was obtained with females bearing only the anterior pair of nipples, which, in a separate experiment, was found to be the most frequently suckled pair. However, females devoid of nipples resumed regular (4-day) estrous cycles between Days 12 and 27 postpartum, in spite of their continuous contact with pups. Thus, when lactation is prolonged beyond the normal time of weaning (Day 21 postpartum), stimulation of the nipples by sucking becomes indispensable for the continued arrest of the estrous cycle. The possible mechanisms underlying this phenomenon are discussed.     

The Effects of Diethylstilbestrol (DES) before Birth on the Development of Masculine Behavior in Juvenile Female Rhesus Monkeys

Eight pregnant rhesus monkeys were injected with 100 μg diethylstilbestrol dipropionate (DESDP) from the 40th day of gestation until term, a long-term treatment. Male (n= 3) and female (n= 5) offspring were obtained. Five other pregnant females were injected with DESDP beginning on the 115th day of gestation and continuing until either the 140th day or term—a relatively short-term treatment. Five female infants were obtained from these short-term treatments. Monkeys from the treated pregnancies were assigned randomly to mother–infant social groups containing untreated male and female infants the same age. They were observed in their peer groups each weekday from 3 to 12 months of age, and the display of mounting and play behavior was recorded for each subject. Results showed that DESDP significantly increased the frequency of display of these juvenile behaviors only in long-term-treated females. However, one of the aspects of mounting that is characteristic of males (the ratio of complete to abortive mounts) was unaffected even by the long-term treatment. Thus, DESDP-treated females displayed a limited behavioral masculinization. Whether this limitation was due to dosage and/or timing or to a selective action of DESDP was not determined. DESDP-treated males were not altered in any measurable way compared to untreated males.     

An experimental examination of female responses to infant face coloration in rhesus macaques

In many primates, infants possess distinctive coloration that changes as a function of age. This colour is thought to serve the purpose of eliciting caretaking behaviour from the mother as well as other conspecifics. The present study investigated the responses of adult female rhesus macaques (Macaca mulatta) to pictures of infant faces in relation to infant age and facial coloration. Study animals were shown digitized images of neonates and 5-6-month-old infants displaying either unaltered facial colour, pink neonatal colour, or novel (green) facial colour. While infant and neonate faces of all colours elicited the attention of adult females, pink neonatal facial coloration did not appear to be especially attractive to subjects in contrast with the findings from an earlier study [Higley, J.D., Hopkins, W.D., Hirsch, R.M. Marra, L.M. Suomi S.J., 1987. Preferences of female rhesus monkeys (Macaca mulatta) for infantile coloration. Dev. Psychobiol. 20, 7-18]. The results suggest that infant facial colour is not particularly important in mediating infant attractiveness to rhesus macaque females as previously suggested or that other infantile facial characteristics might be more important than colour in eliciting caretaking behaviours amongst females.     

Galvanized caging as a potential factor in the development of the "fading infant" or "white monkey" syndrome.

Four rhesus females and their infants were kept in galvanized enclosures, and three were kept in stainless steel caging. All four offspring in the galvanized enclosures developed achromotrichia, alopecia, and weakness that varied from modererate to severe while the three infants in stainless steel cages were clinically normal. Plasma copper, zinc, and iron values as well as liver copper and zinc values of the infants were compared for the two types of caging. Plasma copper values were significantly lower (p less than 0.001) in the animals housed in galvanized cages. Plasma zinc and liver zinc levels were significantly elevated in these same animals (p less than 0.01 and p less than 0.05, respectively). Significant differences were not detected in liver copper values in the two groups of infants. Copper and zinc levels in the dams' plasma and milk were not statistically different between the two groups.