The effects of interspecies infant interaction upon social behavior ofMacaca irus andErythrocebus patas

TwoMacaca irus and twoErythrocebus patas mother-infant pairs were used as experimental subjects to test the effects of interspecies interaction upon social behavior of monkeys. Cynomolgous and patas monkeys given intraspecies interation served as control animals. An unexpected result of this study is that mother-infant behaviors were more affected by interspecies interaction than were infant-infant behaviors. The results indicate that the importance one animal has for another in the development of social behavior depends upon two factors: (a) the behavioral repertoires of interacting animals must be similar and (b) each animal must respond appropriately to the other's behavior.This research was supported in part by National Science Foundation grants No. GB4925 and GB7601 and a grant from the Louisiana State University Graduate Research Council. Animal subjects were provided by the Delta Regional Primate Research Center, United States Public Health Service grant No. FR00164 from the Division of Research Facilities and Resources.The author received personal support while conducting this research as a United States Public Health Service Trainee.     

Effects of group environment on the mother-infant relationship in pigtailed monkeys (Macaca nemestrina)

Behavior of sixMacaca nemestrina mother-infant pairs was observed in two different environments; three pairs were part of a large group in a compound and three pairs were housed in individual laboratory cages. At weeks 14–15 of the infants' lives, group mothers were more retentive of their infants than caged mothers; group infants spent more time in ventral contact with mother and nursed more than did caged infants. The authors conclude that the greater dependence of an infant raised in a potentially dangerous group setting is due to a more protective mother rather than to a more fearful infant.This work was supported by grant no. FR 00166 from the National Institutes of Health, U. S. Public Health Service.Reprints may be obtained from:Primate Information Center, I-321 Health Sciences Building, University of Washington, Seattle, Washington 98105, U.S.A.     

Characterization of obesity in Japanese monkeys (Macaca fuscata) in a pedigreed colony

BACKGROUND: Japanese monkey, Macaca fuscata, is recognized as the monkey species inhabiting the northernmost area in the world, and thus likely to possess unique fat-depositing mechanisms to resist cold weather in winter. We report that obese females are present in the Wakasa group of Japanese monkey reared in an open enclosure of the Primate Research Institute, Kyoto University. METHODS AND RESULTS: Eight of 12 females were categorized as obese, showing percentage body fat of over 22%. The levels of serum leptin (mean +/- SD, 4.9 +/- 2.3 ng/ml) measured in these obese monkeys were significantly higher than those of non-obese peers of the same group (n = 4; 1.2 +/- 0.5 ng/ml) and another Japanese monkey group (Takahama, n = 14; 0.8 +/- 0.25 ng/ml); however, serum levels of adiponectin, insulin, glucose, hemoglobin A1c, and fructosamine did not differ between obese and non-obese monkeys. Few serum lipid parameters such as triglyceride and cholesterol showed lower levels in obese monkeys than their non-obese peers. CONCLUSIONS: These results show that these obese monkeys in the Wakasa group have not developed obesity-related diseases/disorders such as diabetes. In the Wakasa group, the frequency of obese individuals was high in some maternal lineages, suggesting that genetic factors responsible for obesity may have been inherited in these lineages.     

Adult male-offspring play interactions within a captive group of Orang-utans (Pongo pygmaeus)

A family of four Sumatran Orang-utans was studied for three months under captive conditions. Thirty discrete playful interactions between a 19-year-old male and his four-year-old male offspring were analyzed from films and notes. Ten behaviors occurred in a typical play-bout, the most frequent of which were hand contact and mouth contact. Developmental studies of the motor patterns involved in orang-utan social behavior are greatly needed, as the orang is the least understood of the great apes. This research is supported by the following sources: National Institute of Health grants to the Emory University experimental psychology program (H0 00208) and to the Yerkes Regional Primate Research Center (HD00165), and a faculty research grant to the third author from Emory University's McCandless Fund for Biological Research.     

Effects of rearing on aggression and subordination in papio monkeys

The objective of this study is to assess the effects of short-term maternal deprivation (birth to 12 weeks) followed by peer group rearing on the development of aggressive and subordinate behaviors in papio monkeys (superspecies – Papio cynocephalus). Nursery reared monkeys (34 males and 30 females) were compared with mother-peer reared monkeys (11 males and 12 females) in late infancy (6 to 12 months of age) and at the end of their juvenile stage (36 to 42 months of age) in social groups composed of 75% nursery reared subjects and 25% mother reared subjects. Focal animal data were analyzed with a repeated measure ANOVA model. In general, the nursery reared infants tended to be less aggressive than mother-peer reared infants and performed less dominance behaviors, such as displace. Significant sex differences were present in the performance of aggressive (♂ > ♀) and subordinate (♂ > ♀) behaviors. Significant age differences were observed, with infants having consistently higher rates of performance.     

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.     

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.     

A descriptive analysis of gut microbiota composition in differentially reared infant rhesus monkeys (Macaca mulatta) across the first 6 months of life

The gastrointestinal microbiome is recognized as a critical component in host immune function, physiology, and behavior. Early life experiences that alter diet and social contact also influence these outcomes. Despite the growing number of studies in this area, no studies to date have examined the contribution of early life experiences on the gut microbiome in infants across development. Such studies are important for understanding the biological and environmental factors that contribute to optimal gut microbial colonization and subsequent health. We studied infant rhesus monkeys (Macaca mulatta) across the first 6 months of life that were pseudo‐randomly assigned to one of two different rearing conditions at birth: mother‐peer‐reared (MPR), in which infants were reared in social groups with many other adults and peers and nursed on their mothers, or nursery‐reared (NR), in which infants were reared by human caregivers, fed formula, and given daily social contact with peers. We analyzed the microbiome from rectal swabs (total N = 97; MPR = 43, NR = 54) taken on the day of birth and at postnatal Days 14, 30, 90, and 180 using 16S rRNA gene sequencing. Bacterial composition differences were evident as early as 14 days, with MPR infants exhibiting a lower abundance of Bifidobacterium and a higher abundance of Bacteroides than NR infants. The most marked differences were observed at 90 days, when Bifidobacterium, Lactobacillus, Streptococcus, Bacteroides, Clostridium, and Prevotella differed across rearing groups. By Day 180, no differences in the relative abundances of the bacteria of interest were observed. These novel findings in developing primate neonates indicate that the early social environment as well as diet influence gut microbiota composition very early in life. These results also lay the groundwork for mechanistic studies examining the effects of early experiences on gut microbiota across development with the ultimate goal of understanding the clinical significance of developmental changes.     

Reactions of nuclear-family–reared rhesus macaques to the births of younger siblings

A group of juvenile rhesus macaques (Macaca mulatta) living in a nuclear-family laboratory environment was studied to determine their responses to the births of siblings. The frequencies of interactions with family members (mothers, fathers, and new siblings) and nonfamily (peers, unrelated infants, and unrelated adults) were studied over both the year preceding and the year following sibling birth. The frequencies of specific behaviors in each of those interactions and the frequencies of interactions in each area of the nuclear-family unit (home cage, play area, or other families' cage) were also examined. After new siblings arrived, several measures of interactions with mothers, fathers, and new siblings increased significantly; by contrast interactions with peers decreased substantially over the post-birth year. Although the frequency of interactions in home cages remained stable over the 2-year period, interactions outside of the subjects' home cages decreased significantly after siblings were born. An additional subject group whose mothers became pregnant but failed to deliver viable offspring showed no significant changes in total levels of interactions with peers; they did, however, exhibit increases in some interactions with unrelated infants and adults. Female juveniles interacted with new siblings significantly more often than did males when siblings were less than 6 months old, but as siblings grew older (6–12 months), females' levels of interaction with them fell to a level equal to that of males. In the nuclear-family social structure, the birth of a sibling resulted in an increased emphasis on family interactions at the expense of peer interactions.     

Ultrastructural immunocytochemical localization of luteinizing hormone-releasing hormone (LH-RH) in the median eminence of the guinea pig

Summary LH-RH was localized at the ultrastructural level in axons and nerve terminals of the median eminence of the male guinea pig. LH-RH positive neuronal profiles were most concentrated in the medial-dorsal aspect of the infundibular stalk and in the post-infundibular median eminence at the level immediately following separation of the stalk from the base of the brain. LH-RH containing axon profiles were most abundant in the palisade zone; nerve terminals in contact with the hypophysial portal vasculature were relatively rare. The hormone was present within granules that measured 900–1,200 Å in axons of the palisade zone and 400–800 Å in nerve terminals abutting on the portal plexus. The differently sized granules represent heterogeneous populations.Supported in part by U.S. Public Health Service grant HD-09636 from the National Institutes of Health and RR-00167 to the Wisconsin Regional Primate Research Center from the National Institutes of Health. Primate Center Publication No. 15-031The authors wish to thank Dr. Sandy Sorrentino, Jr. for the gift of antiserum to LH-RH and Dr. Ludwig Sternberger for the peroxidase.antiperoxidase complex     

Photoperiodic determination of insect development and diapause

Summary The Photoperiodic Determination Model proposed earlier (I, II) is further elaborated, and its applicability to nondiel photoperiods tested. Model-generated predictions of diapause incidences were in good agreement with observed incidences among larvae of the European corn borer,Ostrinia nubilalis, reared under photoperiods from 15 to 50 hrs duration with scotophases of from 9 to 18 hrs.Research supported by the College of Agricultural and Life Sciences, University of Wisconsin, and by a research grant (GM-07557) from the National Institutes of Health.     

Infant stumptailed macaques reared with mirrors or peers: Social responsiveness,attachment, and adjustment

Comparisons of activity toward mirrors and peers in infant macaques being reared with one of these stimuli as the primary rearing partner revealed markedly greater social responsiveness to a fully accessible cagemate than to one's own reflection. Measures of exploration, aggression, and especially play all revealed the cagemate to be the more potent social stimulus. Mirror-reared infants given additional experience of a live peer behind a transparent partition were less responsive to the mirror than were infants with no social stimulation other than a mirror. In contrast, cagemate-directed behavior of peer-reared infants was not seriously affected by additional exposure to a mirror. A fully accessible peer also elicited more social responding than a peer behind a transparent partition, and infants with experience of both a live cagemate and mirrors were generally more responsive toward the former. Greater agitation in peer-reared than in mirror-reared stumptailed monkeys during separations from their rearing partners suggests that exposure to the physically accessible partner led to stronger attachments. Infants reacted positively to a moderately unfamiliar environment but showed behavioral disruption when placed in a very unfamiliar environment. Disruption was especially evident in peer-reared infants, in which exposure to the unfamiliar environment was compounded with the absence of the attachment figure. Mirror-rearing appeared to reduce the tendency toward ‘isolation syndrome’ behaviors compared to alone-rearing, and these behaviors appear to be less common in stumptailed than in rhesus macaques.     

抱崽与否对笼养雌性食蟹猴个体社会行为的影响

目的比较笼养雌性食蟹猴抱崽与否,是否对其社会行为有影响。方法从2010年5月开始,在江苏省苏州中科实验动物有限公司猴场可观察的个体中,随机抽取观察对象40个;同年10月开始正式拍摄,样本中,11个个体抱崽,29个个体未抱崽。三名观察员采用焦点观察法,使用高清摄像机,对所有个体每天跟踪拍摄7个时间片段,每个时间段为30分组,每个个体观察4 d,共计完成有效累积观察时间560 h;将每天所拍摄视频汇总而后随机分配给NOLDUS分析员分析转换成为行为数据。结果抱崽个体多数时间是怀抱住幼崽,社会友好行为较多,比如为其他个体理毛或被其他个体理毛;社会地位较高,如与猴王共坐于制高点(悬于空中的板子或链子上,依据各个猴场饲养条件而议)时间较长;通讯行为较多,即努嘴行为;运动行为和交配行为较多;而未抱崽个体聚温行为较多,即与其他个体相互怀抱聚温;两组在摄食行为、发情行为、休息行为、冲突行为、警戒行为和各种自我行为差异无显著性。结论抱崽对雌性食蟹猴的社会行为有影响。     

Photoperiodic determination of insect development and diapause

Summary The Dual System Theory of photoperiodic determination was found to be consistent with experimental data on diapause induction in response to skeleton photoperiods. Symmetrical and asymmetrical skeleton photoperiods of both diel and nondiel durations were investigated. The theoretical model was shown to predict accurately the incidence of diapause among larvae of the European corn borer,Ostrinia nubilalis, that had been reared under the different photoperiodic regimes.Research supported by the College of Agricultural and Life Sciences, University of Wisconsin, and by a research grant (GM 07557) from the National Institutes of Health.     

Notes on the development of a mother-reared orang-utan: The first six months

Reproductive behavior is a topic of extreme importance in the literature of primate behavior. This report concerns the mother-infant interaction system in a captiveborn, mother-reared infant orang-utan during the first six months of its life. Of particular interest are the sexual behaviors directed by the mother toward the infant, and the regular stimulation of the infant's genitals. The behaviors described herein are compared to other mother-infant pairs of this and other anthropoid species. This research has been supported by grants from the National Institutes of Health to the Yerkes Regional Primate Center (RR00165), the Emory University Psychology Department (HD00208), and a faculty research grant to the first author from Emory University's McCandless Fund for Biomedical Research.     

Age-related changes in hematological and serum biochemical values in cynomolgus monkeys (Macaca fascicularis) bred and reared using the indoor individually-caged system

Blood samples were collected from 1000 or more apparently healthy cynomolgus monkeys of different ages. All the monkeys had been bred and reared under uniform environmental conditions at the Tsukuba Primate Center for Medical Science, NIH, Japan. Biochemical and hematological data were determined with these samples. The calculated arithmetic means and standard deviations were listed for each item of measurement performed (Tables 3, 4 and 5). The correlation between the obtained value and the age was analyzed using a statistical significance level of 0.1% (Table 6). It was revealed that hemoglobin concentration, mean corpuscular volume, alubuminglobulin ratio and triglyceride concentration increased with age, whereas red blood cell count and serum alkaline phosphatase activity decreased with age in both sexes.     

A comparison of hematological and serum biochemical values between two groups of female cynomolgus monkeys reared under different conditions

The influence of long term rearing conditions on the hematological and serum biochemical values in laboratory-bred female cynomolgus monkeys (Macaca fascicularis) was studied under the following two conditions. Group A: New born infants were nursed by their mothers for at least 12 weeks after birth. After weaning, four monkeys of approximately equal age and body weight were kept in a relatively small cage (90 cm W x 60 cm D x 60 cm H) and reared to five years of age. These rearing conditions are commonly used in the breeding program of our primate center. Group B: One male and five females of wild origin were introduced into a relatively large cage (180 cm W x 180 cm D x 160 cm H). Female monkeys born in these cages were used in this study. All of them were reared by their own mothers and grew well in these cages. Male monkeys born in these cages were removed at about 3.5 years of age. Hematological and serum biochemical values between the two groups in each age class were compared and analyzed by the canonical discriminant analysis (the discriminant analysis with reduction of dimensionality). Age correlated highly with the value of the first canonical variate. The second canonical variate detected a difference in the blood hematology and biochemistry probably induced by the difference in rearing conditions.     

Effect of LSD-25 on mitotic and meiotic chromosomes of mice and monkeys

Summary Chromosomal studies were carried out in bone marrow and testes of mice treated with lysergic acid diethylamide (LSD-25) in acute and chronic experiments, in blood cultures of rhesus monkeys (Macaca mulatta) treated with LSD-25 in vitro, and in blood cultures and testicular preparations of rhesus macaques treated with LSD. No increase in chromosomal damage was observed in bone marrow or testes, but all blood cultures treated with LSD in vitro and some of the blood cultures from rhesus macaques treated in vitro showed a significant increase in chromosomal breaks and rearrangements.Publication No. 397 of the Oregon Regional Primate Research Center, supported in part by Grants No. F00163 and MHI12214 of the National Institutes of Health.     

Growth in Howler monkeys

Howler monkeys (Alouatta caraya) were studied in northern Argentina and subjected to complete post-mortem examination in connection with field observations of atherosclerosis. In order to estimate age of the animals, data was obtained on gross body dimensions, dental age, and organ weights in 298 animals covering the range of about 1–10 kg. The animals were divided into four size groups, and into male, non-pregnant and pregnant female categories. Statistical parameters were obtained for relative organ weights, organ allometry coefficients, gross body lengths, a body length formula based on the Ponderal Index and dental age. The parameters from howlers were compared with those for rhesus monkeys, chimpanzees, human and general primate organ allometric formulas, and differences due to sex and pregnancy reviewed. It is concluded that the growth pattern in howlers is rather similar to that reported for other primates, which makes it possible to estimate maturity satisfactorily, but that further methods must be developed for post-maturity dating.Publication No. 190 of the Oregon Regional Primate Research Center, Beaverton, Oregon, supported in part by Grants FR 00163 and GM 13605 of the National Institutes of Health.