The influence of rank on affect perception by pigtailed macaques (Macaca nemestrina)

Previous studies of affect perception in nonhuman primates have involved young animals and/or manipulations of early experience. Based upon data suggesting that middle-ranked monkeys in small social groups show patterns of behavior different from their low- or high-ranked counterparts, the current study examined the role of social rank in affect perception by normally reared, adult female pigtailed macaques. Employing color videotapes as the presentation medium, we observed animals as they watched unfamiliar animals display social (aggressive or submissive) or nonsocial behavior. Virtually all threats were recorded as the subjects watched the submissive presentations, and most submissive signals occurred while watching aggressive behavior tapes. Middle-ranked monkeys were most attentive during all presentations, and levels of disturbance behavior were related to rank of the watcher and type of presentation observed. The results suggest that dominance status is an influence in the process of affect perception.     

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.     

Population organization of wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra

A field study on wild pig-tailed macaques was conducted in West Sumatra, Indonesia, during three periods from January 1985 to February 1987. During the nine months of the first two periods, unprovisioned monkeys were traced and observed. During the eight months of the last period, monkeys were provisioned and observed mainly at baiting sites. Three troops and ten solitary males appeared at the two baiting sites. Some males immigrated into and emigrated from the troops. The troops had a multi-male multi-female composition. The size of the various troops was 74, 49, and 81 individuals, respectively, and the mean adult sex ratio in the troops was 1:6.3; that is, markedly biased towards females. The home ranges of two of the troops overlapped considerably. When the troops encountered each other at the baiting sites, a clear dominance relationship was recognized. The troops differed in their integration as ranging units: two of the troops did not form subgroups (temporary fission and fusion of each troop), while the other troop frequently split into subgroups. Recent field studies on pig-tailed macaques have suggested a multi-leveled society with harem-type unit groups. However, in the present study, the troops observed had neither a substructure similar to harem-type groups nor a superstructure that emerged as a result of fusion of the troops. The unit group of the pig-tailed macaques appears to be a multi-male, matrilineal group.     

Social stimuli as incentives for delayed response performance by infant pigtailed macaques (Macaca nemestrina)

Six pigtailed macaque monkeys (Macaca nemestrina), ranging in age from 4.5 to 13.5 months, were studied longitudinally on a delayed response procedure in a spatial choice apparatus. In each trial the subjects were exposed to two stimulus animals, an unfamiliar adult female and a familiar age-mate. Prior work showed that such nursery-reared infants overwhelmingly prefer a familiar peer over an unfamiliar adult female. Therefore, the peer was considered to be a positive incentive and choosing the peer was defined as the “correct” response. After the infants were given visual exposure to the stimulus animals, an opaque door was lowered to block them from the subject's view. Then a single delay period of 0, 5, 15, 60, 120, 240, or 480 sec was introduced during 20-trial sessions. The delays were increased over sessions, with about two weeks between sessions. The subjects reliably chose the familiar peer after delays of up to 60 sec, with one subject maintaining correct choices even after 8-min delays. These results revealed that the delayed response performance of young macaques with social incentives was as good as, or better than, maximum performance levels reported for macaques with food incentives. Cues such as odors, sounds, and visual-postural orientation sets could not explain the performance levels at long delays found in this study.     

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.     

Excessive ovarian follicular development in pregnant pigtailed macaques (Macaca nemestrina)

To evaluate the status and possible control of ovarian follicular development during pregnancy, circulating levels of estrone (E₁), estradiol-17β (E₂), and follicle-stimulating hormone (FSH) were measured throughout gestation in both intact and ovariectomized pregnant pigtailed monkeys (Macaca nemestrina). From an additional group of pregnant monkeys, ovaries were obtained at late gestation (on day 150 or 159 of pregnancy) for histological studies. Circulating concentrations of E₁ and E₂ increased on day 13 and remained elevated for about 10 days; they then declined and reached low levels on day 32 of gestation. After day 60, there were gradual but smaller increases in estrogen levels to day 140, after which both E₁ and E₂ levels increased significantly, reaching maximum levels (E₁ = 832.2 ± 210.8 pg/ ml; E₂ = 1.66 ± 0.32 ng/ml) at the end of pregnancy. Removal of ovaries on day 35 of gestation did not affect pregnancy or the pattern of estrogen secretion. Serum concentrations of FSH demonstrated only minor fluctuations during pregnancy but were similar to those found during the early follicular phase of cycling pigtailed monkeys investigated in this study. Ovarian histology revealed extensive follicular growth; in addition to the corpus luteum of pregnancy, ovaries were packed with pre-antral, small antral, and medium-sized Graafian follicles. Some of these follicles appeared to be cystic and showed various degree of atresia; their general appearance was similar to the follicles of human females with polycystic ovary syndrome. Our data suggest that FSH may initiate ovarian follicular growth during gestation. High levels of estrogens were incapable of suppressing FSH secretion but may be responsible for the induction of atresia in a large number of follicles in pregnant pigtailed monkeys.     

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.     

Visual recognition in infant pigtailed macaques after a 24-hour delay

Comparative studies of memory in monkey and human subjects suggest similarities in visual recognition memory across human and nonhuman primates. In order to investigate developmental aspects of visual recognition memory in monkey infants, the familiarization-novelty procedure, developed for use with human infants, was employed with pigtailed monkey infants to study long-delay recognition memory. Subjects were familiarized with a black-and-white abstract pattern. Twenty-four hours later they were tested with the familiar pattern paired with a novel one. Results indicated a significant visual preference for the novel stimulus, providing evidence for recognition memory. These results parallel those obtained with human infants, suggesting further similarities in the development of visual recognition memory.     

Risk factors for dystocia in pigtailed macaques (Macaca nemestrina)

Dystocia (difficult labor) is an important component of the management of nonhuman primates and results in significant fetal and maternal morbidity and increased use of veterinary resources. Dystocias can arise from abnormalities of the maternal pelvis or fetus or uncoordinated uterine activity. Although risk factors for stillbirths have been established in nonhuman primates, risk factors for dystocias have not. The objective of this study was to determine maternal and fetal risk factors for dystocia in macaques. Retrospective data were collected from 83 pigtailed macaques (Macaca nemestrina) diagnosed with dystocia. The diagnosis of dystocia was made based on clinical or pathologic evidence. Maternal records of age, reproductive history, experimental history, clinical records, and fetal birth weight and any applicable fetal necropsy reports were reviewed. The gestational age of the fetus, the infant's birth weight, total previous births by the dam, and the proportions of both viable delivery (inverse effect) and surgical pregnancy interventions (direct effect) in the dam's history generated a model that maximized the experimental variance for predicting dystocia in the current pregnancy and explained 24% of the dystocia deliveries. The number of total previous births and proportion of previous cesarean sections accounted for the greatest effect. This model can identify individual dams within a colony that are at risk for dystocias and allow for changes in breeding colony management, more intense monitoring of dams at risk, or allocation of additional resources.     

Amyloidosis in pigtailed macaques (Macaca nemestrina): pathologic aspects

The pathologic aspects of 248 cases of amyloidosis in pigtailed macaques (Macaca nemestrina) at the Washington Regional Primate Research Center from 1971 through 1985 were studied. Amyloid was present in the spleen, liver and gastrointestinal (GI) tract, either alone or in combination, in nearly 75% of the monkeys. Its occurrence declined with age in the spleen and the GI tract, but increased with age in the liver. Both intestinal inflammation and retroperitoneal fibromatosis were strongly associated with amyloid deposition in the GI tract. Monkeys with histopathologic findings of enteritis or enterocolitis and glomerulonephritis were at increased risk of developing amyloidosis. Forty cases of amyloidosis with a history of chronic diarrhea had type AA amyloid by histochemical tests.     

Amyloidosis in pigtailed macaques (Macaca nemestrina): epidemiologic aspects

A retrospective study of amyloidosis in pigtailed macaques (Macaca nemestrina) at the Washington Regional Primate Research Center (WRPRC) was conducted. Between 1971 and 1985, 248 of 1,952 (13%) necropsies revealed amyloidosis in pigtailed macaques. The influence of demographic factors, diseases and experimental interventions on amyloidosis was examined. Univariate analyses, using two controls for each case, indicated that age, sex, birthplace and residence were related to amyloidosis. After adjusting for age, females were not at greater risk. However, monkeys born at the WRPRC were at greater risk and monkeys 0 to 5 years old residing at the breeding colony were at greater risk than monkeys at the research center. After adjustment for age, monkeys were at greater risk of developing amyloidosis if they had a history of episodes of diarrhea, respiratory disease or trauma. As the number of episodes increased, the risk increased. Monkeys with retroperitoneal fibromatosis, a manifestation of simian D retrovirus infection, were also at greater risk. Using logistic regression and controlling for age, sex, birthplace and residence, monkeys with diarrhea remained at an elevated risk for amyloidosis. Compared with a model combining diarrhea, respiratory disease, septicemia, surgery, trauma and retroperitoneal fibromatosis, a model with diarrhea alone accounted for most of the increased risk.     

Sires influence fetal death in pigtailed macaques (Macaca nemestrina)

Computerized colony records were used to identify dams and sires whose reproductive histories while breeding in harem groups indicated high or low risk for producing fetal deaths. The monkeys were then singly caged and bred within and between risk conditions during 24- to 72-hour matings. Although the low- and high-risk sires did not differ in ability to achieve conceptions, the results revealed that reproductive history predicted subsequent fetal death rates, and sires made a substantial contribution. Overall, high-risk sires had a 4.86 times higher relative risk of producing fetal death than low-risk sires. Compared with this figure, high-risk dams had only a 2.64 times higher risk for fetal death than low-risk dams. The male effect was most evident in comparisons of between- and within-risk matings. Females with excellent reproductive histories experienced a threefold increase in fetal deaths when mated with high-risk males, whereas females with poor reproductive histories experienced almost a 50% reduction in fetal deaths when mated with low-risk males. The results show that male factors beyond fertility need to be considered when examining the causes of reproductive failure in captive primates.     

Infant abuse associated with psychosocial stress in a group-living pigtail macaque ( Macaca nemestrina) Mother

This study reports a case of infant abuse by a pigtail macaque mother living in a captive social group. Patterns of abusive behavior appeared three weeks after the birth of the infant and were in strict temporal as sociation with the repeated kidnapping and severe harassment of the infant by the alpha-female in the group. Before and after the period of social stress, the mother exhibited proper caregiving behavior towards her infant. The analysis of the abusive mother's style of interaction with her infant relative to three control mothers indicated that she was an extremely permissive mother. It is argued that the mother's failure to adapt her mothering style to better protect her infant during the period of repeated kidnappings and the resulting lack of control over the situation may be the mechanism by which stress precipitated infant abuse. © 1994 Wiley-Liss, Inc.     

Nineteen new microsatellite DNA polymorphisms in pigtailed macaques (Macaca nemestrina)

Microsatellite loci known to be polymorphic in baboons (Papio hamadryas) and/or humans were tested in pigtailed macaques (Macaca nemestrina) from the Washington Regional Primate Research Center. Nineteen polymorphisms were identified in the macaques, with an average of 9.2 alleles per locus and an average heterozygosity of 0.76. Seven loci were analyzed using radiolabelled PCR primers and standard gel electrophoresis. Twelve loci were studied using fluorescently labelled primers and the Perkin-Elmer ABI 377 genotyping system. Of these 19 pigtailed macaque polymorphisms, 12 were used to perform paternity testing among captive animals. In a set of 15 infants, this panel of 12 genetic polymorphisms was sufficient to establish paternity in all cases. The number of alleles per locus in pigtailed macaques was compared with the number of alleles in a sample of baboons, and no significant correlation was observed. This indicates that population genetic processes such as genetic drift and recurrent mutation act rapidly enough on these loci to eliminate any relationship in levels of polymorphism across those two species. These 19 loci will be valuable for a range of genetic studies in pigtailed macaques, including paternity testing, analysis of population structure and differentiation among wild populations, and genetic linkage mapping.     

Parturition in Macaca nemestrina

Measures were taken on 187 pregnancies of 104 pig-tailed macaques (Macaca nemestrina) to document the normative course of parturition and to identify factors correlated with high risk for poor pregnancy outcomes. Analyses involved weekly physical examinations and diurnal sleep-wake-fulness patterns during trimester three; behavior during labor and delivery; and newborn sex, Apgar ratings, birthweight, and reflexes. Onset of labor was estimated at three–four hours before delivery, the time when circadian activity level first deviated from its predelivery pattern. Active labor averaged 92 minutes, and was characterized by increased uterine contractions and manipulation of the vaginal area. The modal delivery time was 2200 hr through 2400 hr. Most infants emerged from the vulva in a cranial-anterior-anterior presentation, with only a brief pause between head expulsion and complete emergence. Females with histories of poor pregnancy outcomes were more likely to deliver after midnight and showed less labor-unique behavior than females with good outcome histories. Infants of high-risk females that were delivered after midnight had lower Apgar scores and more bruising than infants of low-risk females delevered before of after midnight, suggesting that high-risk females may have more difficult deliveries. Overall, the results show that simple direct observations of parturition can yield important quantitative normative information that is correlated with reproductive risk factors.     

Enhanced replication of HIV-1 in vivo in pigtailed macaques (Macaca nemestrina)

Non-human primate models for acquired immunodeficiency syndrome (AIDS) are important for studies of prevention and intervention strategies. Ideally, such models would make use of human immunodeficiency virus type 1 (HIV-1) and animals that are readily available for research. HIV-1 was obtained from an infected macaque, and passaged sequentially in three groups of two Macaca nemestrina neonates each. Evidence for enhanced viral replication was first found in one of the group 2 animals, and in both group 3 animals. Observations that underlie this conclusion are sustained viral recovery from peripheral blood mononuclear cells (PBMCs), increased and accelerated production of antiviral antibodies, and the ability to detect plasma viral ribonucleic acid (RNA) months after infection. There was no evidence of CD4 depletion in any of the animals during the follow-up period. These data suggest that a useful non-human primate model for AIDS can be attained in pigtailed macaques (M. nemestrina).     

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.     

Personality traits of adolescent pig-tailed monkeys (Macaca nemestrina): An analysis of social rank and early separation experience

Personality ratings of ten adolescent pig-tailed macaques (Macaca nemestrina) were carried out by three experienced observers who used a simple three-point rating system. A modification of Stevenson-Hinde & Zunz's [1978] procedure, the agreement between raters on each of 21 traits was evaluated. When correlated with social rank, it was shown that dominant animals were rated as being, for example, confident, effective, and opportunistic. Subordinant monkeys were rated as insecure and dependent. Rank correlated negatively, however, with observers' impressions of popularity. Subjects who had undergone a brief maternal separation were rated as less sociable than their nonseparated counterparts. Furthermore, rank-related traits corresponded well with the three personality components that were derived by Stevenson-Hind & Zunz [1978]; this suggested that clusters of traits reliably accompanied and/or contributed to the attainment of social rank.     

Factors associated with intestinal amyloidosis in pigtailed macaques (Macaca nemestrina).

Factors associated with intestinal amyloidosis in pigtailed macaques (Macaca nemestrina) were studied in 74 cases at the Washington Regional Primate Research Center. The medical records of monkeys during the 5-year period from 1983 to 1988 were analyzed to determine the age at death, age at first episode of diarrhea, number of episodes of diarrhea, episode and cumulative duration of diarrhea, and etiologies of diarrhea. Univariate analysis, using one control for each case, indicated that only episode duration was related to intestinal amyloidosis. Affected monkeys had significantly longer mean episode durations of diarrhea. None of the etiologies examined--bacteria, protozoa, fungi, and simian retrovirus--were significant risk factors for amyloid deposition in the intestinal tract.     

Enhanced replication of HIV-1 in vivo in pigtailed macaques (Macaca nemestrina)

Non-human primate models for acquired immunodeficiency syndrome (AIDS) are important for studies of prevention and intervention strategies. Ideally, such models would make use of human immunodeficiency virus type 1 (HIV-1) and animals that are readily available for research. HIV-1 was obtained from an infected macaque, and passaged sequentially in three groups of two Macaca nemestrina neonates each. Evidence for enhanced viral replication was first found in one of the group 2 animals, and in both group 3 animals. Observations that underlie this conclusion are sustained viral recovery from peripheral blood mononuclear cells (PBMCs), increased and accelerated production of antiviral antibodies, and the ability to detect plasma viral ribonucleic acid (RNA) months after infection. There was no evidence of CD4 depletion in any of the animals during the follow-up period. These data suggest that a useful non-human primate model for AIDS can be attained in pigtailed macaques ( M. nemestrina ).