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.     

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.     

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.     

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.     

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.     

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).     

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.     

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 ).     

Blood groups of pig-tailed macaques (Macaca nemestrina).

The human-type A-B-O blood groups of 57 pig-tailed macaques (Macaca nemestrina) were determined and the calculated gene frequencies, O = 0.8908, A = 0.0825 and B = 0.0267, gave excellent fit with the hypothesis of inheritance by triple allelic genes. In tests for simian-type blood groups with rhesus, baboon and crab-eating macaque immune antisera, it was shown that the red cells of pig-tailed macaques are polymorphic for several simian-type specificities defined by those cross-reacting sera. Pig-tailed macaques share with other macaque species the complex Drh-graded blood group system, which seems to occupy a special role among red cell antigens of macaques. Normal sera of three female macaques contained spontaneous isoagglutinins which selectively agglutinated the red cells of some pig-tailed as well as stump-tailed macaques.     

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.     

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.     

Genetics and caging type affect birth weight in captive pigtailed macaques (Macaca nemestrina)

The heritability of birth weight was estimated in 3,562 captive pigtailed macaques using 30 years of breeding and pedigree records. Based on a pedigree of over 12,000 animals, quantitative genetic analyses were performed using statistical variance decomposition methods. The model included additive genetic effects, cytoplasmic genetic effects, birth environment, shared maternal environment, and unmeasured environmental effects. The results demonstrated a strong (h(2) = 0.51) heritable component of birth weight overall, and included significant additive genetic heritability (h(2) = 0.23), and cytoplasmic heritability (h(2) = 0.09). In addition, a significant effect of birth location and cage type was identified, explaining an additional 6% of birth weight variance. The use of a nonhuman primate model for studying the effects of genes on birth weight eliminated many of the problems associated with confounding variables in human studies, and allowed for the quantification of a heritable component of birth weight.     

Development of dermal ridges in the volar skin of fetal pigtailed macaques (Macaca nemestrina)

Development of the dermal ridges in volar skin was investigated in 28 pigtailed macaque (Macaca nemestrina) fetuses of known gestational age, ranging from 51 days postconception to newborn. Histology, scanning electron microscopy, and staining of the abraded dermal surface were used in the study. Morphological features of the dermal-epidermal system and their changes with advancing age are described. Chronology was established for stages in the development of the volar skin, i.e., the differentiation of the primary and secondary epidermal ridges (PER and SER) at the undersurface of the epidermis corresponding to the formation of primary and secondary dermal ridges (PDR and SDR) and the development of the dermal papillae. PDRs were first seen at 55 gestational days and SDRs at 93 days. Differentiation of sweat ducts occurred over the period between 60 and 119 gestational days. A regional sequence of differentiation starting with the digital apices of the hand and ending in the calcar area and the phalanges of the foot was documented. Generally, morphogenesis in the macaque was accelerated relative to that in the human fetus by approximately 3 weeks.     

Weaning, body weight, and postpartum amenorrhea duration in pigtailed macaques (Macaca nemestrina)

Early permanent infant separation or weaning decreases the time interval between pregnancies and interbirth intervals for many female primates. At least part of the interpregnancy interval consists of postpartum amenorrhea, a period of non-menstruation lasting from the time of birth until the female begins to ovulate. This study investigated the effects of weaning age and dam's body weight on the duration of the interval between pregnancies, the duration of postpartum amenorrhea, and the number of cycles to conception in a year-round breeder. Female pigtailed macaques (Macaca nemestrina) have an observable perineal swelling that fluctuates throughout the menstrual cycle and provides a means of detecting ovulation. The perineal swelling records of socially housed pigtailed macaques were studied from July 1996 to September 1998. Postpartum amenorrhea data were obtained on 44 females who gave birth to normal, viable infants. As weaning age increased and dam's weight decreased, postpartum amenorrhea, and consequently the interval between pregnancies, increased in duration. The interpregnancy interval consisted almost entirely of the postpartum amenorrhea phase. Our finding that a higher dam's body weight decreased the length of postpartum amenorrhea duration lends support to the hypothesis that a minimum body weight is necessary for menstrual cycles to occur. Most females became pregnant on their first ovulation regardless of weaning age and whether or not they were carrying an infant. As the weaning age of the infant and the dam's weight increased, ovulation went from occurring after separation to occurring before separation.     

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.     

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.     

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.