Effects of parity and age on female attraction to faces of infants and neonates in rhesus macaques

This study investigated the effects of parity and age on female rhesus macaque attention toward infants, and assessed whether the faces of neonates are more attractive than those of older infants. Six nulliparous and six multiparous females were shown digitized images of neonates’ and 5- to 6-month-old infants’ faces. Attention and preferences for images were measured by gaze duration and other picture-directed behaviors, including lip smacking, approaches, and presentations. As predicted, nulliparous females displayed significantly longer gaze durations for images than did multiparous females. There were no significant differences in gaze duration for faces of neonates and those of infants, but images of infants were approached more frequently than images of neonates. This difference is tentatively explained on the basis of differences in female familiarity with neonates’ and infants’ faces and differences in opportunities for allomothering with neonates and infants.     

Control of nipple and body contact by mothers and infants in rhesus macaques.

While 3-month-old infant rhesus macaques (Macaca mulatta) were awake and active in social interactions away from their mothers, body and nipple contacts with their mothers were nevertheless made from time to time. In each dyad the proportions of contacts made by the mother nearly equalled those broken by her, suggesting a meshed interaction in which each partner accepted most of the other's contact initiations and terminations. Passive prevention of nipple contact by a mother reduced the frequency of nipple contact by her infant in the first 5 s after the infant had made body contact. Passive prevention occurred after fewer than 1 in 6 body contacts initiated by infants, and--even without its occurrence--most infants were less ready to take the nipple after their own initiatives than after maternal initiatives. Once nipple contact had been made, the probability of breaking body contact was reduced. The role of maternal rejection both in the control of nipple contact in the short term and in determining (through its effect on the sucking pattern) whether the mother gives birth in the next birth season or later is discussed. We suggest that, by the age of 3 months, the infants had already learned when and how often nipple contact with their mothers would be acceptable during their awake and active periods, and we suggest that subsequent decreases in the frequency of nipple contact were partly the results of maternal rejections which were accepted by the infants.     

Fatal outbreaks of proliferative enteritis caused by Lawsonia intracellularis in young colony-raised rhesus macaques.

Ten juvenile rhesus monkeys (Macaca mulatta) died acutely in two separate disease outbreaks. The animals had segmental thickening of the distal ileum with associated proliferative, rugous appearing mucosae. Microscopically, necrosis, exudative inflammation, mucosal ulceration, and crypt hyperplasia were present. Intracellular organisms were seen histochemically and ultrastructurally, and were confirmed to be Lawsonia intracellularis using a specific immunohistochemical method. Proliferative enteropathic conditions caused by L. intracellularis are reported in an ever-increasing range of hosts, suggesting that the infection may exist unrecognized in an even greater array of species, possibly including man.     

Postpartum recuperation in primiparous rhesus macaques and development of their infants

Female primates endure great costs during pregnancy and lactation. Some studies have been conducted on exploring these; however, information on how maternal condition before conception influences maternal postpartum recuperation and infant development are not well known, especially in primipares. This 2-year investigation explored how maternal condition, maternal foraging time and alert time, and infants' time on nipple influenced postpartum recovery of primiparous rhesus macaques, as well as their infant's development during the first 3 months postpartum. The study was conducted on 11 female rhesus macaques (Macaca mulatta) living at the Caribbean Primate Research Center, Sabana Seca Field Station, Puerto Rico. Infant survivorship and development were not influenced by maternal age at first parturition or by the infants' time on the nipple. Infant development and maternal recovery were influenced by maternal condition before conception. Older primipares demonstrated greater postpartum recuperation. Maternal postpartum recuperation was not influenced by maternal feeding time or time the infant spent on the nipple. Maternal recuperation was negatively correlated with increased vigilance (alert time).     

Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants

A functional polymorphism in the promoter region of the serotonin transporter (5-HTTLPR) gene has been associated with variation in anxiety and hypothalamus-pituitary-adrenal (HPA) axis function in humans and rhesus macaques. Individuals carrying the short allele are at a higher risk for developmental psychopathology, and this risk is magnified in short allele carriers who have experienced early life stress. This study investigated the relationship between 5-HTTLPR allelic variation, infant abuse, and behavioral and hormonal responses to stress in rhesus macaques. Subjects were 10 abusive mothers and their infants, and 10 nonabusive mother-infant pairs. Mothers and infants were genotyped for the rh5-HTTLPR, and studied in the first 6 months of infant life. For mothers and infants, we measured social group behavior, behavioral responses to handling procedures, and plasma concentrations of ACTH and cortisol under basal conditions and in response to stress tests. The proportion of individuals carrying the short rh5-HTTLPR allele was significantly higher among abusive mothers than controls. Among mothers and infants, the short allele was associated with higher basal cortisol levels and greater hormonal stress responses in the infants. In addition, infants who carried the short rh5-HTTLPR allele had higher anxiety scores than infants homozygous for the long allele. The rh5-HTTLPR genotype also interacted with early adverse experience to impact HPA axis function in the infants. These results are consistent with those of previous studies which demonstrate associations between serotonergic activity and anxiety and stress reactivity, and add additional evidence suggesting that genetic variation in serotonergic function may contribute to the occurrence of abusive parenting in rhesus macaques and modulate emotional behavior and HPA axis function.     

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.     

恒河猴离乳幼猴B病毒动态监测

目的调查恒河猴离乳幼猴BV感染的动态变化,探讨早期控制的可能。方法采用BV全病毒为抗原的ELISA试剂盒,对两批离乳后群养的54只恒河猴幼猴每月采血检测BV感染情况,连续检测13个月。结果随月龄的增加,BV感染率上升,其中12月、1月、2月、3月、4月BV阳性猴数量相对增加较明显。结论幼猴性成熟期之前BV感染率超过70％且呈现出一定的变化规律,春、冬季BV的感染率相对较高,应早期加强BV的有效预防控制,降低BV的感染,提高猴群质量。     

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.     

Effect of outbreeding on weight and growth rate of captive infant rhesus macaques

The introduction of unrelated conspecifics into captive groups of primate species is desirable to inhibit inbreeding. However, for many species, such groups increasingly represent highly inbred isolate populations that are analogous to regionally isolated populations of the same species among whom the effects of outcrossing on fitness are unknown. A study of potentially adverse effects of cross-breeding between regionally isolated populations of rhesus macaques was conducted to assess the maximum advantage or disadvantage to be expected for cross-breeding such populations of other cercopithecoid primates. For this purpose, the infant weights and rates of growth of hybrid Chinese/Indian rhesus macaques were compared to those of their nonhybrid Indian peers and to those of consanguineously inbred Indian rhesus macaques from several other captive breeding groups. Neither adverse nor advantageous effects of such hybridization were detected, suggesting that outcrossing between isolates of other cercopithecoid primates with a similar social structure and mating pattern should not affect the fitness of resulting offspring. Since levels of inbreeding are roughly inversely proportional to levels of genetic diversity within populations, such outcrossing should be intensified by zoos and other captive breeding centers to ensure the continued survival of captive species, especially those that are endangered or otherwise irreplaceable.     

Rapid progression is associated with lymphoid follicle dysfunction in SIV-infected infant rhesus macaques

HIV-infected infants are at an increased risk of progressing rapidly to AIDS in the first weeks of life. Here, we evaluated immunological and virological parameters in 25 SIV-infected infant rhesus macaques to understand the factors influencing a rapid disease outcome. Infant macaques were infected with SIVmac251 and monitored for 10 to 17 weeks post-infection. SIV-infected infants were divided into either typical (TypP) or rapid (RP) progressor groups based on levels of plasma anti-SIV antibody and viral load, with RP infants having low SIV-specific antibodies and high viral loads. Following SIV infection, 11 out of 25 infant macaques exhibited an RP phenotype. Interestingly, TypP had lower levels of total CD4 T cells, similar reductions in CD4/CD8 ratios and elevated activation of CD8 T cells, as measured by the levels of HLA-DR, compared to RP. Differences between the two groups were identified in other immune cell populations, including a failure to expand activated memory (CD21-CD27+) B cells in peripheral blood in RP infant macaques, as well as reduced levels of germinal center (GC) B cells and T follicular helper (Tfh) cells in spleens (4- and 10-weeks post-SIV). Reduced B cell proliferation in splenic germinal GCs was associated with increased SIV+ cell density and follicular type 1 interferon (IFN)-induced immune activation. Further analyses determined that at 2-weeks post SIV infection TypP infants exhibited elevated levels of the GC-inducing chemokine CXCL13 in plasma, as well as significantly lower levels of viral envelope diversity compared to RP infants. Our findings provide evidence that early viral and immunologic events following SIV infection contributes to impairment of B cells, Tfh cells and germinal center formation, ultimately impeding the development of SIV-specific antibody responses in rapidly progressing infant macaques.     

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.     

The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.     

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta)

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.     

Delayed imitation of lipsmacking gestures by infant rhesus macaques (Macaca mulatta)

Human infants are capable of accurately matching facial gestures of an experimenter within a few hours after birth, a phenomenon called neonatal imitation. Recent studies have suggested that rather than being a simple reflexive-like behavior, infants exert active control over imitative responses and 'provoke' previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. Here we report that 1-week-old infant rhesus macaques (Macaca mulatta) who show immediate imitation of a lipsmacking gesture also show delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Macaque infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates.