Social development in nursery-reared pigtailed macaques (Macaca nemestrina)

The social development of 240 nursery-reared pigtailed macaques (Macaca nemestrina) was studied from postnatal weeks 4 to 32. The objectives of the study were to document developmental trends and evaluate social behavior in laboratory-reared M. nemestrina raised at the University of Washington Infant Primate Laboratory, and to identify husbandry factors that might affect early social development. Only infants who had not undergone invasive postnatal experimental manipulation and had no chronic illness or injuries were included in the study. Infants were separated from their mothers and housed singly, but had access to peers for 30 min a day, 5 days a week, in a large playroom. Play and social behaviors emerged early in development, increased during the developmental period studied and occupied a large portion of the infants' time budgets. Although disturbance behaviors occurred with some frequency and duration early in development, they occupied a very small portion of the infants' time budget at 8 months of age. Weaning from infant formula at 16–19 weeks retarded development of play behavior. Permanent removal of a cloth comforter (diaper) during weeks 20–24 had no long-term behavioral effects. It was concluded that at 8 months of age these infants showed relatively normal species-typical behavioral repertoires. Am J Primatol 41:23–35, 1997. © 1997 Wiley-Liss, Inc.     

Perinatal hypothermia and maternal temperature declines during labor in pigtailed macaques (Macaca nemestrina)

Body temperature, respiration, and heart rate were recorded for 90 perinatal pigtailed macaques (Macaca nemestrina) within the first hour after birth. Hypothermia and corresponding depressed respiration and heart rate were evident in all animals. Regression analysis revealed that time-since-birth accounted for most of the observed variance in all measures. Temperatures of three pregnant females were monitored during labor and delivery. Declines in maternal temperature during labor suggested that depressed maternal temperature influenced the observed hypothermia in newborns. Increases in ambient (cage) temperatures during labor indicated that the females were emitting heat while declining in temperature.     

Maintenance of high-density lipoprotein blood levels prior to spontaneous abortion in pig-tailed macaques (Macaca nemestrina)

Blood was drawn throughout the first half of the pregnancies of 24 pig-tailed macaques (Macaca nemestrina) to evaluate longitudinal high-density lipoprotein (HDL) changes. In all 15 normal pregnancies, HDL decreased at least 50%; the mean value for the group fell from 0.45 gm/liter to 0.17 gm/liter. HDL began to fall after about four weeks of pregnancy. However, no comparable HDL change occurred in nine pregnancies that terminated in spontaneous abortions. This lack of an HDL decrease was unexpected. Subsequent studies showed that the predominant decrease was in the HDL₂ subfraction. The data indicate that the normal physiologic metabolism or utilization of HDL is aberrant early in pregnancies ending in spontaneous abortions and may be due to a dysfunctional fetal-placental unit.     

Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

Early maternal recognition of offspring vocalizations in rhesus macaques (Macaca mulatta)

This study investigated the development of maternal recognition of infant calls in rhesus macaques (Macaca mulatta). Fifteen mothers and their offspring, of age ranging from several hours to 28 days, served as subjects of an experiment in which the offspring's distress vocalizations were recorded and then played back to their mothers simultaneously with those of an age-matched control infant. The proportion of time looking at, but not the proportion of orientations to the speaker playing the offspring's vocalizations increased significantly as a function of infant age. Specifically, mothers of infants older than 1 week of age responded longer to the playback of their own infant's calls than did mothers of younger infants. These findings provide the firt evidence that offspring recognition in macaques develops between the first and second week of the infant's life and are consistent with the hypothesis that mothers need to be exposed to their infants' calls in order to learn their acoustic characteristics.     

Pair-rearing infant monkeys (Macaca nemestrina) using a “rotating-peer” strategy

Appropriate rearing conditions for captive primates are important for both research and breeding purposes. In an earlier study, pigtailed macaque infants that were pair-reared with a single continuous partner exhibited excessive social clinging and could not adapt to living in large social groups at 8–10 months of age. In the present study, eight macaques were pair-reared until they were 6 months old. Each member of an animal's four-monkey social group served as a home-cage partner. In an attempt to reduce excessive mutual clinging, the pairs were rotated every 2–3 days to increase the variability of social stimulation in the home cage. However, these infants developed abnormal social behaviors that were in some cases even more extreme than those exhibited by infants pair-reared with a single continuous partner. A second goal of this experiment was to study interlaboratory reliability for the development of social behavior. The animals were divided into two groups, one housed in a nursery and the other in a biological safety level 3 virus laboratory. Some differences were detected between the two groups, demonstrating the necessity of controls in biobehavioral developmental research. Am. J. Primatol. 41:141–149, 1997. © 1997 Wiley-Liss, Inc.     

Kin recognition in zebrafish: a 24-hour window for olfactory imprinting

Distinguishing kin from non-kin profoundly impacts the evolution of social behaviour. Individuals able to assess the genetic relatedness of conspecifics can preferentially allocate resources towards related individuals and avoid inbreeding. We have addressed the question of how animals acquire the ability to recognize kin by studying the development of olfactory kin preference in zebrafish (Danio rerio). Previously, we showed that zebrafish use an olfactory template to recognize even unfamiliar kin through phenotype matching. Here, we show for the first time that this phenotype matching is based on a learned olfactory imprinting process in which exposure to kin individuals on day 6 post fertilization (pf) is necessary and sufficient for imprinting. Larvae that were exposed to kin before or after but not on day 6 pf did not recognize kin. Larvae isolated from all contact with conspecifics did not imprint on their own chemical cues; therefore, we see no evidence for kin recognition through self-matching in this species. Surprisingly, exposure to non-kin odour during the sensitive phase of development did not result in imprinting on the odour cues of unrelated individuals, suggesting a genetic predisposition to kin odour. Urine-born peptides expressed by genes of the immune system (MHC) are important messengers carrying information about 'self' and 'other'. We suggest that phenotype matching is acquired through a time-sensitive learning process that, in zebrafish, includes a genetic predisposition potentially involving MHC genes expressed in the olfactory receptor neurons.     

Growth and sexual dimorphism in a population of hybrid macaques

Growth and sexual dimorphism have long been the focus of investigation for researchers interested in the life history and socioecology of nonhuman primates. Previous research has shown that sex differences in the duration of growth, or bimaturism, are primarily responsible for the sexual dimorphism observed in anthropoid primates with multimale–multifemale social structure, such as macaques. The present study investigates sex differences in patterns of craniofacial and somatometric growth relative to head and body size and relative to dental development in a population of hybrid macaques (Cercopithecidae: Macaca ) from Sulawesi, Indonesia. How these patterns may contribute to sexual dimorphism in this hybrid population is also examined. The results of the study suggest that there is no substantial effect on the levels of sexual dimorphism associated with hybridization in these macaques. Although sex differences in patterns of size-related, or allometric, growth patterns play a significant role in the development of sexual dimorphism for some cranial dimensions in these hybrids, bimaturism seems to be the primary component in the ontogeny of sexual dimorphism in this hybrid population. The observed levels of hybrid dimorphism and the predominant ontogenetic pattern of bimaturism characterized by prolonged male growth are consistent with previously published reports on dimorphism and growth in other cercopithecine primates.     

Frequent harassment of mounting after a takeover of a group of moor macaques (Macaca maurus)

Harassment behavior during mounting was observed in a group of moor macaques (Macaca maurus) in Sulawesi, Indonesia. During the study periods in 1994 and 1995, most harassment was performed by juveniles less than 5 years old. No harassment by adult females was observed. Mounting by the α-male, who had newly immigrated to the group, was harassed more frequently than that by the β-male in 1994. In 1995, the frequency of harassment during mounting by the α-male was low as compared with that in 1994. In the case of the new α-male, harassment occurred more frequently during mounting with sexually tumescent females than during mounting with detumescent females. Harassment was rarely observed during mounting by natal males of the group. Many hypotheses have been proposed to explain harassment of mounting in primates. The present results offer support for the following two hypotheses: (1) harassment is an attempt to establish a social bond between the performer and the mounting individuals; or (2) harassment occurs in response to mounting by unfamiliar males.     

Fecal testosterone immunoreactivity as a non-invasive index of functional testosterone dynamics in male Japanese macaques (Macaca fuscata)

Validation of a simple method for the extraction and quantification of testosterone (T) from the excreta of male Japanese macaques (Macaca fuscata) is presented. Radioimmunoassay of paired fecal and serum samples collected from four intact sexually mature males during the breeding season provided profiles that were significantly correlated when samples were offset by approximately 48 hr. Additionally, no significant differences were observed in the pattern of temporal variation of T levels in serum and feces. Two castrated males were injected with radioinert T, and the patterns of excretion were observed by analysis of serial fecal and urine samples. Approximately 48 hr after the steroid was administered, a significant peak in the average fecal T levels was apparent. The injection event was also registered in the urine of both males, although qualitative differences were observed. These data suggest that measures of fecal T provide a reliable and non-invasive means of assessing gonadal function in this species. As the analysis of hormone levels in feces allows for frequent, stress-free sampling with minimal disruption, this method should be preferred in long-term orin situ applications requiring endocrine monitoring.     

A fatal attack on an unweaned infant by a non-resident male in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

A non-resident male attacked a 4-month-old unweaned infant in a free-ranging group of Japanese macaques (Macaca fuscata) and it died 2 days later from a severe wound. When the infant was alone at the feeding site, the non-resident male rushed at it. The infant ran away as soon as it became aware of the male, but was captured. The male bit the infant on its hand, foot, and arm, while continuously scanning his surroundings. He did not kill the infant immediately and, after the infant escaped, he did not chase or attack it at all. Although the infants right arm was bleeding heavily, it survived until the following day. The infanticide occurred a few weeks before the mating season began, so the victims mother soon resumed estrus and the subsequent inter-birth interval was shortened. The first-, second-, and fourth-ranking adult males had died or disappeared a few months before this infanticide, and there were no other group members near the infant when the infanticidal male appeared. The infanticidal male had not been observed before this incident. Compared to one-male groups, the occurrence of infanticide in multi-male groups of Japanese macaques is extremely infrequent. However, in other reports of infanticide in Japanese macaques as well as in this case, it has been noted that infanticide is likely to occur in the pre- or early-mating season, when there are no resident males to defend the infant against attacks, and when a threatening male is least likely to be the infants father.Electronic Supplementary Material Supplementary material is available for this article at     

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.     

The behavior of postreproductive females in a wild population of toque macaques (Macaca sinica) in Sri Lanka

I compared the behavior of three old postreproductive females in a wild population of toque macaques (Macaca sinica)in Polonnaruwa with those of reproductive females via focal-animal sampling techniques. Postreproductives foraged less, slept more, and were less active overall than reproductive females were. They also had significantly lower rates of agonistic behavior, were more peripheral, and had lower frequencies of overall affiliative contact. Although postreproductives initiated contact with others as frequently as reproductives did, group members initiated contact with them significantly less than they did with reproductive females. Postreproductives associated more with adult females than reproductives did and less with adult and subadult males than high-ranking reproductives did. Juvenile and infant females associated more frequently with reproductive females of high or low rank than with postreproductives. Postreproductives resembled low-ranking reproductive females in giving less grooming to others than they received. This contrasts with high-ranking females, which gave more grooming to others than they received. The results suggest that old age and cessation of reproduction are evident through the manifestation of distinct behavioral characteristics in toque macaque females.     

Sex differences in infant integration in a semifree-ranging group of Barbary macaques (Macaca sylvanus,L. 1758) at Salem,Germany

Sixteen multiparous Barbary macaque females with newborns were studied over a 16 month period within the context of their naturally formed group. Analysis of their social behavior revealed 1) triadic interactions involving focal females, their newborns, and other group members occurred mainly with other females; and 2) mothers with female newborns interacted mainly with females of their own matriline, while mothers with male newborns interacted mainly with nonmatriline females. Observed in two successive birth seasons, this pattern indicates that partners of maternal interactions chose each other according to the sex of the newborn. Measures of distance from the mother also reflected differences between infants of different sex. At about five months of age, female infants were observed close to their mothers significantly more often than males. This finding follows the pattern of a sex-specific infant socialization process which integrates female infants into the network of their matrilines and male infants into the broader group. This sex-specific integration pattern is interpreted as supporting female philopatry and male dispersal. © 1995 Wiley-Liss, Inc.     

Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan

The relationships between fruit morphology and the foraging behavior of the Yakushima macaque, Macaca fuscata yakui were studied during a 9-month field study and series of laboratory experiments on Yakushima Island, southern Japan. These relationships may affect seed germination traits through seed dispersal. The macaques foraging behavior was observed in order to obtain data concerning the treatment of pulp and seeds. Seeds in feces and spat seeds were collected and analyzed. A linear discriminant analysis of the data led to the following results: (i) an increase in the relative flesh volume of a fruit was one of the potential factors which increased the probability of seed dispersal by the macaques; and (ii) seed size was an important parameter in relation to the type of seed dispersal (by defecation or spitting out). The germination test was conducted in a laboratory, then the germination rates and delays of dispersed seeds were compared with those of seeds collected directly from trees. The germination of dispersed seeds of Ficus thunbergii, Eurya japonica, and Vaccinium bracteatum, was significantly enhanced by passage through the macaques gut. The enhanced germination behavior was not seen in larger seeds, such as those of Psychotria serpens, Myrsine seguinii, Diospyros morrisiana, and Neolitsea sericea. The germination enhancement in small-seeded plants could be due to a sorting effect from the passage through the gut, which selects seeds with a narrower range of germination traits.     

Interactions among adult males and females before and after the death of the alpha male in a free-ranging troop of Japanese macaques

This report documents the social interactions among adult Japanese macaques in a free-ranging troop before and after the death of the alpha male, who died at 28 years of age after occupying his rank position for 17 years. The alpha male’s physical condition had deteriorated due to his extreme age for several months before his death. However, he maintained his alpha position. When he was attacked by the second-ranking adult male, he was rescued by the alpha female. Thereafter, whenever the second-ranking male approached him, the alpha male screamed for the alpha female’s support. The number of adult females to whom the alpha male maintained proximity during his last four months was similar to that during the same period of the previous year. Prior to his death, the alpha male was observed in close proximity to the alpha female much more frequently than was the second-ranking male. These results indicate that the alpha male maintained his position by depending on female support and particularly that of the alpha female.     

Responses of foster-mothers and troop members to adopted newborns in a captive group of rhesus monkeys

Two rhesus monkey males and two females, born to females caged singly, were exchanged with same-sex infants born to females in a large troop which was held in an enclosure in a different building. The ages of the infants were between 24 and 120 hr. The selected foster mothers (FMs) immediately accepted the foreign infants, allowed them to suckle and treated them as their own offspring. Compared with interactions with previous offspring, the FMs initially tended to be more possessive and restrictive of their foster infants: generally they took longer before they allowed the infants to sit at a distance from them and more readily retrieved them. The foster infants tended to be more active (‘fidgety’) than natural (control) offspring born to the troop. Non-related members of the troop, differentiated between foster and control groups. These troop animals more frequently approached and sat in proximity, often in fur-contact with, touched, groomed, and lipsmacked to, foster infants than control infants. The attractiveness of the fostered infants seemed to be slightly associated with the FMs' dominance rank. The foster infants were therefore viewed by others as having assumed the role afforded by the FMs' rank. Thus both FMs and other troop members recognized the unfamiliarity and novelty of the foster infant but the infants were still accepted into the group. We suggest that the different treatment of the foster infants by the troop may have consequences on the infants' future social development.     

The expression of peptidoglycan recognition protein-S1 gene in the scallop Chlamys farreri was enhanced after a second challenge by Listonellaanguillarum

A more rapid and powerful response against repeated exposure of same pathogen in vertebrates is usually considered as the reflection of immunological memory, but it is not well understood in invertebrates. In the present study, the temporal expression profiles of Chlamys farreri peptidoglycan recognition protein-S1 (CfPGRP-S1) gene after two challenges of Listonella anguillarum were examined to evaluate priming response in scallops. The up-regulation of CfPGRP-S1 mRNA occurred 3 h earlier, and the expression level was significant higher (P < 0.05), after the second challenge than that after the first challenge. The preliminary results provided new insights into invertebrate immunological memory, and they also would be helpful to develop strategies for disease control.