Early rearing experiences and the performance of affinitive and approach behavior in infant and juvenile baboons

We tested the hypothesis that subtle, short-term (birth to 3 months) differences in rearing experiences (peer-peer vs. mother-peer) produce measurable differences in the development and performance of four affinitive and four approach behaviors in late infancy (12 months of age) and in the late juvenile period (42 months of age). Data on 87 monkeys (45 males and 42 females) were obtained by a series of approximately 2,100 focal animal sampling sessions. Significant effects of rearing were found in two affinitive behaviors (Allogroom andHold) with mother-peer reared subjects having a higher mean rate of performance. There were no significant main effects or interactions among any of the approach behaviors. Several suggestions are proposed to account for the resistance of six behaviors (Muzzle-muzzle, Touch, Ear flatten, Follow, Lip smack andSocial approach) to the effects of the experimental procedures: (1) these behaviors may reflect genetically mediated behavioral characteristics of the species that are not modified by environmental conditions; (2) environmental conditions used in the study may have been too subtle and consequently insufficient to produce an effect on relatively resistant behaviors; or (3) effects of the early rearing experience on these behaviors may be observable only during adolescence or adulthood when the proper performance of these behaviors is more crucial to social success, social integration and reproduction. Formerly Southwest Foundation for Research and Education.     

Behavior of nursery/peer-reared and mother-reared rhesus monkeys from birth through 2 years of age

The behavior of 8 nursery/peer-reared and 16 mother-only reared rhesus macaques was observed between birth and 5 months of age, with follow-up studies conducted when the animals were 10–21 months old and living in large social groups. Nursery-reared neonates were more awake, active, and irritable than mother-only reared monkeys. From 1 to 5 months of age the nursery/peer-reared animals exhibited a greater variety of behaviors than the mother-only reared infants, which spent the majority of the time in ventral contact with mothers. As juveniles the groups were indistinguishable with the exception of more self-directed behaviors observed in the nursery/peer-reared monkeys. Both rearing conditions, by virtue of their atypicality, imposed restrictions on social development. The behavioral similarity of the juveniles while in the large social group may be a function of maturation or due to the rehabilitative effect of the large social group.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

Social status,behavior, and central serotonergic responsivity in female cynomolgus monkeys

The relationship between social status, behavioral characteristics, and central serotonergic function was examined in eight adult female cynomolgus monkeys (Macaca fascicularis). The subjects were housed in four-member social groups for 6 months. Social behavior was observed three times a week. The early follicular phase of the menstrual cycle was determined based on the occurrence of menses, and the prolactin response to acute administration of fenfluramine HCl during the early follicular phase was used as a measure of net brain serotonergic responsivity. Delta prolactin responses (the prolactin response to fenfluramine minus baseline concentrations) were lower in dominant than in subordinate females. Dominant females were more aggressive and less submissive than subordinates. Likewise, females with the lowest delta prolactin concentrations were more aggressive and less submissive than females that had relatively large increases in prolactin. Delta prolactin responses also correlated negatively with percent time eating and investigating in close proximity to penmates, and correlated positively with percent time scanning anxiously while alone. The same pattern of correlation was noted between social status and the aforementioned affiliative behaviors. It was concluded that high central serotonergic responsivity may be associated with low rates of aggression, high rates of submission, and subordinate social status in female cynomolgus monkeys. © 1995 Wiley-Liss, Inc.     

Abnormal behaviors in nursery-reared squirrel monkeys (Saimiri sciureus)

Seventeen squirrel monkeys (Saimiri sciureus), 11 nursery-reared and six mother-reared, were monitored to clarify the type and degree of deviant behaviors that result from rearing this species in the nursery. Two observation periods were used: the first when the subjects averaged 6.7 months of age, the second when they averaged 15.5 months. Thirteen activities involving variations of nonnutritive orality, stereotypic posturing, and agitated behaviors were seen in the nursery-reared subjects, but never in the mother-reared subjects. No consistent gender, subspecies, or age differences were evident. Squirrel monkeys, like chimpanzees and some Old World monkeys, do develop atypical self-directed behaviors when deprived of normal stimulation during early development.     

Aggressiveness of male mice: Cooperation between cage-mates

Male mice (Mus domesticus) were reared in groups of 2 or 3 males until 13 weeks of age. They then fought each other every third day. Aggressiveness was quantified on the basis of the frequency of aggressive behavior shown by each mouse in each match. The data suggest that there was positive correlation between the levels of aggression of the cage-mates in the 2-male group. Significant correlations also existed between the most doninant and subordinate males and between the secondary and the subordinate males in the 3-male group. The aggressiveness of male mice correlated positively with that of their cage-mates from 65 to 91 days of age but did not correlate with that of the cage-mate living together from 35 to 61 days of age.     

Habitual hot-spring bathing by a group of Japanese macaques (Macaca fuscata) in their natural habitat

Japanese macaques (Macaca fuscata) in a free-ranging group in Jigokudani valley, Nagano prefecture, are known to bathe in a hot spring. We used scan sampling in a study aimed at elucidating the causal factors and possible social transmission of this behavior. From 1980-2003, 31% of a total 114 females in the group habitually bathed in the hot spring. The habit was more widespread in dominant matrilines than in subordinate matrilines. Infants whose mothers bathed were more likely to bathe than infants of mothers who did not bathe. The number of monkeys bathing was clearly influenced by ambient air temperature. More monkeys bathed in the hot spring in winter than in summer. The results support the thermoregulation hypothesis of hot-spring bathing. Bathing behavior varies among age and sex categories of monkeys, with adult females and juveniles bathing more often than adult males and subadults. We compared hot-spring bathing with other thermoregulatory behaviors in various primate populations.     

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.     

Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys

Thirty years of research on early social and hormonal environments and their relationship to the expression of behavioral sex differences in rhesus monkeys are reviewed. These studies demonstrate that whether aggressive and submissive behaviors are sexually dimorphic depends primarily on the social and not the hormonal environment. Early rearing environments without mothers or allowing brief periods of peer interaction produced higher levels of male aggression and female submission. Presenting behavior was expressed more by females than males in environments with high male aggressivity and female submissiveness. No sex differences in presenting occurred in low aggressivity environments, unless monkeys were reared isosexually, when males presented more than females. Rough and tumble play and foot-clasp mounting were consistently exhibited more by males than females across all rearing environments studied, but rearing environment affected the degree of the sex difference. When reared isosexually males displayed less, and females more, foot-clasp mounting than when heterosexually reared. No social environment increased the low frequency of female rough and tumble play. Suppressing neonatal androgen in males did not effect any sexually dimorphic behavior. Prenatal androgen administration to genetic females masculinized many aspects of their juvenile behavior, consistently increasing rough and tumble play and foot-clasp mounting across different social environments. Thus the sexually dimorphic behaviors which showed the smallest variability across social contexts were the most profoundly affected by the prenatal hormonal environment. These studies demonstrate that the expression of consistent juvenile behavioral sex differences results from hormonally induced predispositions to engage in specific patterns of juvenile behavior whose expression is shaped by the specific social environment experienced by the developing monkey.     

Social and solitary play in a colony of vervet monkeys (Cercopithecus aethiops)

This study describes and defines play in a laboratory colony of vervet monkeys (Cercopithecus aethiops). Play is divided into 26 units of behavior and the frequencies of these behaviors are recorded. Analysis shows that sex, age, and dominance have effects on some play behaviors. The play behavior of each age/sex group within the colony is described both quantitatively and qualitatively. Adult females are characterized by reinforcement of the play of immature monkeys, adult males by rough play with older male juveniles, four-year-old females and three-year-old males by stimulation of play in young infants, and males in general by a preference to play within their peer group. It is suggested that modified repetition of behaviors, diversified interactions, and innovative behaviors, are important qualities of play, and are essential to the adaptive plasticity of behavior in primates.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Sex differences in the behaviour of immature captive lowland gorillas

Studies of the behaviour of 26 (12 males and 14 females) captive infant and juvenile lowland gorillas showed clear sex differences. Females showed greater interest in young infants and were more active in nest building as well as in solitary and social grooming. Males were more active in locomotive, dominance, and aggressive behaviour and in social play. Hand-rearing further increased aggression. Males were more aggressive when they lived with only one partner, and they rose in rank even above older females, a pattern that has not been observed in naturally reared gorillas.     

Long-term effects of social rehabilitation in rhesus monkeys

A group of 19 rhesus monkeys was assembled and observed in a large outdoor pen. Five experimental groups were present: 3-year-old mother-peer reared monkeys, surrogate-rehabilitated isolates, socially-rehabilitated isolates, surrogate-peers (who had served as “therapists” for the preceding group), and 1-year-old mother-peers. The major results indicated first, that the surrogate-rehabilitated isolates played socially significantly less than both mother-peer groups, and second, that the group as a whole seemed to display an abnormally low overall level of behavior. Possible interpretations and theoretical implications are discussed. Request reprints fromMark S. Cummins, Department of Psychology, McGill University, Montreal, Quebec, Canada.     

The influence of target sex and dominance on evoked attack in Rhesus monkeys

Attack behaviors were elicited by the electrical stimulation of the hypothalamus of freely moving male rhesus monkeys. The influence of the sex and dominance status of target animals on the evoked response was measured. Animals offered as targets were dominant males and females and subordinate males and and females. Males were attacked more often than females and subordinate targets of either sex were attacked more often than dominant targets. A comparison was made between spontaneous and evoked attack behavior.     

非优势顺位雄性黄山短尾猴的交配策略

在多雄多雌、顺位决定交配机会、雄性偏斜繁殖的非人灵长类社会中,低顺位雄性为提高自己的繁殖成功率,通常采取多样的交配策略以获得较多的交配机会。对非优势顺位雄性交配策略的研究可以增加对灵长类社会性行为复杂性的理解,对于深入探讨动物的婚配制度及繁殖策略具有十分重要的科学意义。本研究采用目 标动物取样法和全事件记录法,在２０１２ 年９ －１２ 月（交配期）记录了安徽黄山短尾猴鱼鳞坑ＹＡ１ 群中４ 只成年雄性个体的交配及有关的行为。研究发现：（１）非优势顺位雄性个体在远离优势顺位雄性视野范围的交配频次和交配时间显著高于优势顺位视野范围内;（２）与优势顺位雄性个体相比,非优势顺位雄性的强行交配（forced copulation）和隐秘交配（clandestine copulation）比例较高;（３） 就交配对象而言,对成功生育的雌性个体,优势顺位雄性在选择交配对象时具有明显的倾向性,非优势顺位雄性在选择时倾向性不显著;对未生育的雌性,优势顺位雄性更倾向于选择没有生殖经历的亚成年雌性个体,非优势顺位雄性则倾向于选择处于哺乳后期的成年雌性个体;（４）在具体交配策略上,优势顺位雄性选择跟随（follow） 雌性,非优势顺位雄性则通过做鬼脸 （grimacing）和性追求（sexual chasing）直接获取交配机会。本研究结果表明黄山短尾猴中非优势雄性个体形成了多变的交配策略,更多采取强制性方式,以获得更多的交配机会,多数的交配都是机会性的。     

Social and reproductive behaviors in surrogate-reared squirrel monkeys (Saimiri sciureus).

A colony of 16 surrogate-reared squirrel monkeys was observed for the adequacy of social and reproductive behaviors at maturity. Aside from some self-directed abnormalities centering around nonnutritive orality, this group was behaviorally normal in spite of having no contacts with mother-reared, older conspecifics. Half (N=5) of the females gave birth, with four infants viable. One infant has remained with the colony and is thriving. The other three remained with the group for as long as 42 days before death or removal. Maternal care appeared adequate. Mean estimated conception age for females was 35 months, and the mean impregnation age for males was estimated to be 42 months.     

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157–170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.     

Peer separation in infant chimpanzees,a pilot study

Seven nursery reared chimpanzees (Pan troglodytes), 7.5 to 10.5 months of age, were studied to determine the effects of a short period of separation from their peers on behavior and heart rate. The chimpanzees were separated from their mothers at birth, and reared in the nursery in a group living environment. The experiment encompassed a 13-day period, including 4 days of normative baseline, 5 days during which three of the infants were separated and housed in isolation while the other four controls remained together, and 4 days in which all of the animals were reunited. Six quantified behavioral observations and five heart rate measurements were obtained daily. Following separation, the isolated infants were behaviorally agitated, and exhibited increases in vocalizations, rocking and self-clasp behaviors, as well as changes in facial expression including cry face, whimper face and pout face. Time spent locomoting decreased in all seven animals during the separation period. Agitated behavior in the separated and isolated infants alternated with stationary withdrawn behavior. Individual differences were prominent. Heart rate was notable by the generally poorly developed circadian rhythmicity throughout the 13 day period; significant HR changes did not appear otherwise associated with separation. Day three of separation appeared to represent a point of transition with stereotyped motor behaviors developing in the three isolated infants and in one control infant.     

The impact of paternity on male–infant association in a primate with low paternity certainty

In multimale groups where females mate promiscuously, male–infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male–infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate‐guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi‐free‐ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male–infant interactions were affiliative, indicating the rareness of male–infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male–infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male–infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low‐cost paternal care.