Sexual behavior in a captive group of pigtailed monkeys (Macaca nemestrina)

Sixteen pigtailed monkeys (Macaca nemestrina) were studied to determine patterns of estrous cycles and sexual behavior. The average estrous cycle lasted 42 days, the average tumescent period 21 days, and the average quiescent period 17 days. Results are consistent with those obtained from studies of individually caged monkeys. The mean length of gestation for five live births was 174.6 days with a range of 167 to 179 days. Patterns of heterosexual, homosexual, and self-oriented sexual behavior are described and quantified.Mating behaviors of Japanese and pigtailed monkeys were compared. Although individual elements of sexual patterns were similar, there were quantitative differences and differences in the temporal patterning of the behavior.Supported by Grant FR 00166 from the National Institutes of Health, United States Public Health Service.     

Determinants of dominance hierarchy in a captive group of pigtailed monkeys (Macaca nemestrina)

Eighteen pigtailed monkeys, all strangers to each other, were placed together in a laboratory compound. Two infants were eliminated from the study shortly after group formation. To determine dominance hierarchy aggressive-submissive interactions were observed among the remaining 16 monkeys during 4 periods covering 5 months of group development.Results suggested that 3 factors were basic determinants of dominance hierarchy: body weight for males, estrus for females, and maturity for both sexes.Aggressive-submissive interactions were far more frequent during Period I, the first hour of group formation, but decreased with stabilization of hierarchical order in subsequent periods.Aggressive-submissive interactions were not evenly distributed among all possible pairs in the group, but tended to involve mostly the high-ranking animals. Also, high-ranking animals concentrated their aggression towards more submissive monkeys of their own rank. Because low ranking animals were involved in fewer aggressive-submissive interactions, their rank determination was difficult.This research was supported by grant No. FR-00166 from the National Institutes of Health, U. S. A.     

Assessment of obesity in pigtailed monkeys (Macaca nemestrina).

Obesity was studied in a colony of 873 Macaca nemestrina to establish tools for epidemiologic studies, to examine a genetic form of obesity, to document age/sex relationships to obesity, and to compare metabolic profiles of obese and normal monkeys. Age/weight growth curves were analyzed to select the most obese monkeys and age- and sex-matched normal controls. Degree of adiposity was determined using tritiated water for estimation of lean body mass. Body weight, anterior trunk height, and abdominal and triceps skinfolds were measured. Fasting insulin, fasting free fatty acids, and glucose disappearance rate were determined. The results give evidence of similarities between macaque and human obestiy.     

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.     

In vitro fertilization in the pigtailed macaque (Macaca nemestrina)

The objective of this study was to investigate the possibility of collecting oocytes and semen from pigtailed macaques (Macaca nemestrina) and to establish a protocol for the production of viable embryos that would be suitable for transfer into surrogate females. A total of 82 oocytes were collected from a total of four females (on 2 d with two females each). Semen was collected from the same male on both occasions with respective ejaculate volumes of 0.55 and 0.1 mL containing 2 x 10(9) and 6.6 x 10(8)sperm/mL. Following insemination and after 48 h in culture, 42 (51.2%) of the oocytes had cleaved. Of these, 21 were selected based on developmental stage and their morphology and cryopreserved. The remainder was kept in culture for an additional 5 d, at which time three had reached the expanded blastocyst stage. A total of five transfers were performed with frozen-thawed embryos; two of these resulted in pregnancies and the birth of infants. The results of this study demonstrated that oocytes can be retrieved from pigtailed macaques and that such oocytes can be inseminated and cultured in vitro to the blastocyst stage and give rise to viable offspring after transfer into surrogate females.     

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.     

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.     

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.     

Heterochrony and sexual dimorphism in the pigtailed macaque (Macaca nemestrina)

Somatic growth is not a simple linear process with a constant rate of growth. The most successful attempts to quantify growth as a function of age or size have employed nonlinear techniques. Sexual dimorphism of primate growth, weight vs. age, was examined using nonlinear models with Sirianni and Swindler's ([1985] Growth and Development of the Pigtailed Macaque, Boca Raton, FL: CRC Press) growth data on the pigtailed macaque (Macaca nemestrina). The best fit of several exponential growth models was the Gompertz curve: Different multiple phase models were also fit, where each phase represents a distinct exponential component. The two-phase models proved to be the best (R² = .0.84 for females, 0.91 for males), suggesting that there are two growth spurts, one in infancy and one at puberty. The timing of the beginning and end of the first spurt is the same in males and females, but the rate, and value of the asymptote for this phase, is greater in males. The timing of the second spurt is earlier, and the rate of growth for this spurt is smaller in females than males. The sexual dimorphism in these species is not a simple rate change, but a complex interaction of timing and rate over the entire period of growth. It would be impossible to separate these entities with a linear, polynomial, or single-phase model of the data. While these data and results complement much of the existing work on adult dimorphism, they also emphasize the vital role that ontogenetic data have in elucidating the underlying evolutionary mechanisms that generate sexual dimorphism. © 1994 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.     

Responses to urinary stimuli in pigtailed (Macaca nemestrina) and stumptailed (Macaca arctoides) macaques

Responses to different urine samples were studied in pigtailed (M. nemestrina) and stumptailed (M. arctoides) macaques. Both species exhibited more interest towards urine samples from their own species than neutral stimuli. Responses towards urine samples from other macaque species did not significantly differ from those towards neutral stimuli. In stumptailed macaques, no differential interest was observed between urine samples from a known (the adult male of the group) and an unknown adult male conspecific.     

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.     

Intraspecific red cell enzyme variation in the pigtailed macaque (Macaca nemestrina)

The erythrocytes of 350 pigtailed macaques (Macaca nemestrina) were examined for electrophoretic variation of hemoglobin and 26 enzymes. Seven enzymes showed variation in more than 1% of individuals: phosphoglucose isomerase, phosphoglucomutase-1, soluble NADP-dependent isocitric dehydrogenase, peptidase A, peptidase C, 2,3-diphosphoglycerate mutase, and acid phosphatase. Variation with lesser frequency was found in soluble glutamic-oxalacetic transaminase, phosphoglycerate kinase, lactic dehydrogenase, and hemoglobin. Only eight samples were tested for esterase D, and one of these had a variant phenotype. Enzymes with no clear variation were adenylate kinase, adenosine deaminase, phosphofructokinase, hexokinase, pyruvate kinase, glyceraldehyde 3-phosphate dehydrogenase, aldolase, phosphoglycerate mutase, phosphopyruvate hydratase (enolase), phosphoglucomutase-3, and superoxide dismutase. There was father-to-son transmission of PGI, PGM-1, peptidase C, 6PGD, 2,3-DPGAM, NADP-ICD, and acid phosphatase variants, suggesting that these loci are autosomal as in man.     

Aggression in pigtailed macaque (Macaca nemestrina) breeding groups affects pregnancy outcome

Past research has shown that aggressive behaviors can affect female reproductive outcome in nonhuman primate captive breeding programs. In this study, aggressive behaviors were recorded in a colony of pigtailed macaque monkeys (Macaca nemestrina) and related to pregnancy outcome. For 22 weeks, behavioral data were collected from nine breeding groups, consisting of zero to one male (some males were removed after a cycle of conceptions for husbandry reasons) and four to eight females. Observations included all occurrences of 11 aggressive behaviors during 15 min observation sessions, 1-3 times a week. Mean weekly aggression levels during the study period were determined for each group as well as for each pregnancy. Aggression data were summarized with Principal Components Analyses. Results indicate that pigtailed macaque aggression falls into five distinctive categories: warn, engage, threaten, pursue, and attack. Breeding groups differed in their levels of aggression, even after controlling for group size, presence of a sire, and group stability. Levels of the five aggression categories were found to affect the probability that a pregnancy ended in either a natural birth of a live infant, a clinical intervention producing a live infant, or a nonviable outcome. The predictive value of aggression was significant when clinical interventions were included as possible reproductive outcomes. Behavioral observation of captive groups could identify "risk" conditions affecting pregnancy outcome and the requirement for clinical intervention.     

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).     

Relationships between faces and body motor patterns in a group of captive pigtailed macaques (Macaca nemestrina)

The paper describes facial displays and body motor patterns observed in a group of five captive pigtailed macaques during dyadic aggressive and courtship interactions. Correlations between facial displays and body motor patterns were studied quantitatively in order to establish the predictive value of a facial display for the behaviour of the performer. Results indicate that each of the facial displays is largely restricted to a certain type of interaction. Within an interaction of a certain type, the facial displays provided a rather precise prediction of how the performer continued the interaction. Furthermore, the predictive value varied quantitatively between subjects addressing the same partner as well as within the subject when addressing different partners. It is argued that various faces probably function as much as a signal to the interaction partner as to the other individuals which are likely to be nearby and might interfere with the interaction.     

Spatial organization of captive monkeys (Macaca nemestrina)

An artificial group of 18 pigtailed monkeys, selected by sex and size (age) to simulate the composition of natural groups of macaques, was formed. All were strangers to each other. Observations were made over five months. Data on the monkeys' resting and clustering locations in the compound were analyzed in two ways. Spatial organization emerged about one month after the group was formed when the group acquired a competent leader. The leader, certain high ranking females, and/or females in estrus were seen consistently in a geographically central area of the compound and therefore were termed central monkeys. This central subgroup, coherent in terms of area and roles, persisted throughout the study. Development of increased group structure was also indicated by increased stability of dyadic affectional relationships. The study indicates that social organization of the pigtailed macaque will develop when some of the environmental and prior experience variables are controlled. The results highlighted the leader's role and suggest that it is at least as essential in social organization as kinship and factors inherent in a natural environment. Estrous cycles of females and seasonal variations of temperature in the compound were other factors affecting spatial and social relationships of the group members.     

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 ).