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.     

A comparison of primiparous and multiparous mother-infant dyads inMacaca mulatta

The relationships of 42 rhesus monkey mother-infant dyads were examined to investigate the effects of the mothers' parity. Primiparous mothers were found to be younger, more excitable and less confident than the multiparous mothers. They also received more aggression from other adult females living in their social group and were more anxious about their infants, approaching and leaving them more frequently. The primiparous mothers protected their daughters more than the multiparous mothers and their daughters correspondingly spent more time in the ventro-ventral position and more time on the nipple. Their sons however spent less time in contact with their mothers than did the sons of the multiparous mothers. Although the primiparous mothers protected their daughters more than their sons, for the multiparous mothers the converse was true and sons received more maternal protection. It is suggested that the greater protectiveness of the multiparous mothers towards male infants may be a consequence of the interest siblings have in males, whereas the greater protectiveness of primiparous mothers to daughters may stem from their greater vulnerability to attacks from adult females. The importance of mother-mediated sibling influences may explain the lack of strong parity differences in previous studies.     

Maternal Behavior and Infant Congenital Limb Malformation in a Free-Ranging Group of <Emphasis Type="Italic">Macaca fuscata</Emphasis> on Awaji Island,Japan

We studied the relationship between maternal behavior and infant disability in 12 mother-infant dyads for the first 5 weeks of infant life in the free-ranging Japanese macaque (Macaca fuscata) group on Awaji Island, Japan, from May to September 2001. Congenital limb malformations are prevalent in this population, and as such carry implications for behavior and conservation. We did not detect any differences in maternal activity budgets, mother-infant physical contact, infant holding, and overall nursing and infant transport time between mothers of non-disabled infants, disabled infants that were able to cling to their mothers, and disabled infants whose limb structure prevented clinging. Mothers of infants with limb malformations severe enough to prevent normal clinging behavior manually supported their infants during nursing and locomotion significantly more than other mothers did theirs. Increased support-carrying and support-nursing, and higher frequencies of holding the infant to one's ventrum, suggest that mothers of extensively malformed infants may be investing more to facilitate the survival of their offspring and that infant disability appears to be influencing maternal behaviors in this population.     

Adoption by captive parturient rhesus macaques: Biological vs. adopted infants and the cost of being a “twin” and rearing “twins”

Four rhesus macaque (Macaca mulatta) mothers each spontaneously adopted and reared an abandoned, unrelated neonate in addition to their own neonate. Data on relative time spent in maternal contact and who maintained proximity were collected for the biological and adopted “twins” and singleton control infants using focal animal sampling. Infant weight gain and the subsequent conception history for each mother were obtained for the following year. Biological infants spent more time in maternal contact than their adopted “twin” siblings. When in contact with their mothers, biological “twins” spent more time in the ventro-ventral position and more ventral time alone than adoptees. Mothers initiated more contacts with their biological infants than their adopted infants, suggesting these differences may be due to differential maternal behavior. “Twins” gained weight at a slower rate than singletons, and mothers rearing “twins” produced significantly fewer offspring the following season. Am. J. Primatol. 43:259–264, 1997. © 1997 Wiley-Liss, Inc.     

Neural and environmental factors impacting maternal behavior differences in high- versus low-novelty-seeking rats

Selective breeding of rats exhibiting differences in novelty-induced locomotion revealed that this trait predicts several differences in emotional behavior. Bred High Responders (bHRs) show exaggerated novelty-induced locomotion, aggression, and psychostimulant self-administration, compared to bred Low Responders (bLRs), which are inhibited and prone to anxiety- and depression-like behavior. Our breeding studies highlight the heritability of the bHR/bLR phenotypes, although environmental factors like maternal care also shape some aspects of these traits. We previously reported that HR vs. LR mothers act differently, but it was unclear whether their behaviors were genetically driven or influenced by their pups. The present study (a) used cross-fostering to evaluate whether the bHR/bLR maternal styles are inherent to mothers and/or are modulated by pups; and (b) assessed oxytocin and oxytocin receptor mRNA expression to examine possible underpinnings of bHR/bLR maternal differences. While bHR dams exhibited less maternal behavior than bLRs during the dark/active phase, they were very attentive to pups during the light phase, spending greater time passive nursing and in contact with pups compared to bLRs. Cross-fostering only subtly changed bHR and bLR dams' behavior, suggesting that their distinct maternal styles are largely inherent to the mothers. We also found elevated oxytocin mRNA levels in the supraoptic nucleus of the hypothalamus in bHR versus bLR dams, which may play some role in driving their behavior differences. Overall these studies shed light on the interplay between the genetics of mothers and infants in driving differences in maternal style.     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Effects of nonmaternal restraint on the vocalizations of infant rhesus monkeys (Macaca mulatta)

This study explored the effects of restraint by females other than the mother on the vocalizations of infant rhesus macaques (Macaca mulatta) in a captive social setting. In this species, females are very attracted to young infants and will frequently approach, groom, and hold the infant. Incompetent handling, abusive behavior, or extended periods away from the mother that prevent the infants from nursing represent potentially significant risks for infants. Vocal responses to such risky conditions appear to be the infants' only means to promote a return to their mothers. We examined the association between the severity of the threat posed to the infant and the nature of its vocal response to restraint, and whether the infants' calls influenced the behavior of their mothers or captors. The results suggest that situations posing greater risks for the infants, i.e., longer periods of restraint, were associated with a greater use of noisy screams. Furthermore, mothers' responding was associated with a greater use of noisy screams as well. The mothers' reactions, however, could be described as cautious, and consisted mostly of closer monitoring; such tempered response might be related to the risk of injury to the infant that could result from a more forceful and direct attempt at retrieval.     

Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment

The behavioral and adrenocortical responses of rhesus macaque mothers to a series of four consecutive 4-day separations from their 5-month old infants in an unfamiliar environment were examined. A biphasic behavioral response to separation was observed, with passive behavior, locomotion, and vocalization highest on Day 1 of separation, and self-directed behaviors and environmental exploration peaking during Days 2–4. Stereotyped locomotion increased, and passive behavior decreased, across successive weeks of separation. The rhesus mothers exhibited substantial cortisol elevations one and two hours postseparation, with cortisol decreasing on the fourth day of separation. The cortisol response was strongest during the first week of separation, but robust elevations occurred in response to repeated separations. No signs of behavioral depression were observed. The results indicate that infant separation combined with removal to a novel environment can be a potent stressor for rhesus macaque mothers.     

Serotonin transporter allelic variation in mothers predicts maternal sensitivity, behavior and attitudes toward 6-month-old infants

Maternal behavior in the new mother is a multidimensional set of responses to infant cues that are influenced by the mother's early life experiences. In this study, we wanted to test if mothers' early life experiences and mothers' genotype have interactive effects on maternal behaviors and attitudes, something which has not been previously explored. In a sample of 204 mothers, we assessed maternal genotype at the serotonin transporter-linked polymorphic region (5-HTTLPR) and an adjacent upstream polymorphism (rs25531), together giving rise to three alleles: short (S), L(G) and L(A). Controlling for maternal age and parity, we showed that this genotype can predict differences in maternal sensitivity at 6 months postpartum: mothers with an S (or the functionally similar L(G)) allele were more sensitive than mothers who lacked the allele during a 30-min recorded mother-infant interaction (F (4,140) = 3.43; P = 0.01). Furthermore, we found highly significant gene-environment interactions in association with maternal behavior, such that mothers with no S or L(G) alleles oriented away more frequently from their babies if they also reported more negative early care quality (F (5,138) = 3.28; P = 0.008). Finally, we found significant gene-environment associations with maternal attitudes; mothers with the S allele and with greater early care quality scored higher on ratings of their perceived attachment to their baby (F (5,125) = 3.27; P = 0.008). The regression results show significant interactions between the reported quality of care mothers received from their own parents and genotype on both their frequency of orienting away from the infant during the interaction (F(5, 138) = 3.28; P = 0.008, Fig. 1a) and their perceived attachment feelings to the infant (F(5, 125) = 3.27; P = 0.008, Fig. 1b); however the direction of the effects for these two outcome measures were different from one another. With increasing care quality, mothers with the L(A)L(A) genotype (no S or L(G) allele) oriented away less frequently, while S or L(G) allele carriers showed no significant change. In contrast, with increasing early care quality. L(A)L(A) (no S or L(G) allele) mothers scored lower on perceived attachment to their infants, whereas S or L(G) allele carrying mothers scored higher. [corrected].     

Feeding tactics in juvenile rhesus monkeys (Macaca mulatta)

In a group of rhesus monkeys, feeding tactics of juveniles were studied in a competitive situation in which food presentation had been modified, and where food was supplied in a feeding trough six times a day. Juvenile offspring of high-ranking mothers remained longer in the feeding area gathering food. In contrast, juvenile offspring of low-ranking mothers went less often to the feeding area, primarily to collect food. Low-ranking juveniles also gathered the food faster than did dominants and used longer feeding bouts. High-ranking juveniles interrupted their feeding more spontaneously than did subordinate ones. Low-ranking juveniles did so more often as a result of avoiding and being startled. Juvenile males entered the feeding area to satisfy their food requirements more often than females, but were also aggressively expelled more than females. No relation was found between age in months of juveniles and any feeding parameters or causes of interruption. Nor were significant differences found between young and old juveniles. Juvenile rhesus appear to use different tactics in accessing food according to their sex and to their mothers' dominance rank.     

Motherless mothers revisited: Rhesus maternal behavior and rearing history

Classic studies have demonstrated that isolation- and peer-rearing in infancy can result in overt deficits in maternal behavior in rhesus monkeys, although nonmother-reared monkeys may become adequate caretakers if allowed experience with infants. Maternal styles in normally-reared mothers have been reported to vary widely. In the present study, the range of maternal proficiency of nonabusive, nonrejecting nonmother-reared mothers was examined. The behavior of mother-reared, peer-reared, and isolate-reared multiparous mothers was observed and compared for the first six months following parturition. Both peer-reared and isolate-reared mothers exhibited differences in maternal behavior from mother-reared mothers. Inasmuch as variations in maternal behavior may impact on the infant, investigators should be aware of the rearing histories of females used as breeders in the laboratory.     

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.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

How rhesus monkey infants budget their time between mothers and peers

Social play between two rhesus monkey (Macaca mulatta) infants takes place mainly when they are both not in body contact with their mothers. This suggests that social play and mother-infant body contact are potential competitors in the infants' time budgets. We investigated whether the presence of a playmate changed the duration of mother-infant body contact during the first 6 months of life. A decrease in contact would favour play opportunity. Mother-infant pairs were observed alternately alone and together with another pair. Resting, which always occurs during on-mother, was not reduced in the presence of a peer. Body contact during activity phases was reduced in most playing pairs, but only to a large extent in pairs which showed relatively high levels of contact in the situation without a peer. Play opportunity was further increased by synchronization of the rest-activity cycles of the two infants; this occurred without a reduction in mother-infant interactions. No influences by mothers on play opportunity were demonstrated, except that strong maternal interference with resting reduced activity synchronization.     

Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year

A review of the literature suggested that animals exposed to more risk in their social groups should be more enterprising. Rhesus monkey infants of 37 to 44 weeks were attracted to bait in places out of their mothers' reach. The tests were run in the home pen, in the absence of social companions apart from a sibling in its second year of life, if present. In each test the bait was a sawdust and grain mixture, with two or three raisins, and enterprise was measured in terms of the number of raisins taken. Before the test period, the infants had lived in small stable captive social groups. Infants of non-top-ranking mothers took more raisins than infants of top-ranking mothers, if infants subject to high levels of aggression from their own mothers or from the adult males in their groups, were excluded. Observations of the group in a competitive foraging situation confirmed that non-to-ranking infants should be at greater risk than top-ranking ones. The infants receiving notably high levels of aggression from their mothers or the adult males in their groups took more raisins than the remainder. These results are consistent with the view that experience of risk in a social group can promote enterprise in rhesus monkey infants of less than a year old. The problems of assessing “risk” faced by socially living animals, and the mechanisms whereby experience of risk could enhance enterprise, ere discussed.     

Comparison between wild-born mother-female infant interactions and laboratory-born mother-female infant interactions during the first 14 weeks after birth in individually caged cynomolgus macaques

In this study we compared mother-female infant interactions between primiparous and multiparous laboratory-born (F1) cynomolgus macaques (Macaca fascicularis) in individual cages at Tsukuba Primate Center (TPC), Japan, during the first 14 weeks of infant life. We also compared interactions between multiparousF1 mothers and their female infants with those between wild-born mothers and their female infants when mothers and their infants were housed in the same individual cages. PrimiparousF1 mothers showed significantly higher values for contact with and holding of their infants than multiparousF1 mothers. The primiparousF1 mothers also tended to behave aggressively toward their infants when the latter did not show any obviously irritating behaviors. Thus, the primiparousF1 mothers seemed to be inconsistent in terms of maternal behavior. Compared with multiparous wild-born mothers, multiparousF1 mothers moved more frequently, held their infants less frequently and acted aggressively toward their infants less frequently. However, infants ofF1 mothers, as well as infants of wild-born mothers, interacted with their mothers through approaching and playful contact with them. These findings indicate that the attitude of multiparousF1 mothers toward their infants was relatively passive. Possible reasons for the passive maternal style of multiparousF1 mothers are discussed.     

川金丝猴非母亲照料行为的影响因素及其母亲获益——以神农架川金丝猴投食群为例

灵长类社会中存在着非母亲成员(成年雌猴、青少年猴和成年雄猴)对婴儿的照料行为,即非母亲照料行为,该行为直接影响新生婴儿的存活与发育以及婴儿母亲的日常活动,是灵长类学研究领域的热点问题.本研究于2019年3月至2019年11月,采用焦点动物取样和瞬时扫描取样,探究了川金丝猴非母亲照料行为的影响因素及其对母亲活动分配的影响...     

The relationship between maternal rank and companion choice in immature macaques (Macaca mulatta andM. radiata)

Eight bonnet and eight rhesus macaques, ranging from 5–8 months of age, were observed with respect to their choices of companions. These data were then correlated with the dominance ranks of the mothers of the companions involved. Preliminary results showed that the maternal ranks of the rhesus infants were significantly correlated with the maternal ranks of their companions; no such correlation could be demonstrated for the bonnet monkeys. Thus the partner choices of rhesus infants appeared to be more constrained than were those of the bonnets. The results were discussed in relation to the social systems of bonnet and rhesus macaques. Supported in part by faculty research grant D-552, Chancellor's Patent Fund DG #44, and by RR00169 to the California Primate Research Center.     

The development of range of action in infant cynomolgus monkeys (Macaca fascicularis) reared by restrained mothers

In order to study the effects of the mothers' range of action on the development of their infants' range of action during the first year of life, mother cynomolgus monkeys were restrained in their range of action by penning them in a separation cage within the large cage of the harem group they belonged to. The infants, however, could leave their mothers' separation cage. The control group consisted of infants growing up with unrestrained mothers in the same group. It appeared that infants of restrained mothers were initially retarded in the development of their range of action but at the end of the first year they did not differ anymore from infants of unrestrained mothers. It is concluded that the maternal range of action only temporarily affects the development of the infant's range of action.     

Benefits to Female Helpers in Wild Rhinopithecus roxellana

To assess what female Sichuan snub-nosed monkeys (Rhinopithecus roxellana) gain from allowing others to care for their infants, we collected behavioral data on 12 mother-infant dyads at Zhouzhi National Nature Reserve in the Qinling Mountains, China. Mothers’ feeding time significantly increased when infants were cared for by other group members versus when they were cared for by the mothers themselves. The time mothers spent autogrooming and receiving grooming also increased when they were temporarily relieved of maternal duties; however, mothers did not groom other individuals more when they were not encumbered by infants. There are several benefits that mothers gain from having helpers care for their infants: They gain more time to feed and thus increase their feeding efficiency. Mothers have more time to engage in hygienic and maintenance activities because they autogroom and receive allogrooming more. Lastly, mothers save energy when their infants are with helpers. Wild Sichuan snub-nosed monkey mothers meet their basic survival and maintenance needs because of helping behavior.