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.     

Correlation of perineal detumescence and ovulation in the pigtail macaque (Macaca nemestrina).

A study was made of the relationship between ovulation and perineal detumescence in the pigtail macaque (Macaca nemestrina). Daily laparoscopic examation of both ovaries was made beginning on the 9th day of the menstrual cycle. The appearance of the ovaries was recorded and photographs were taken of the perineum and ovaries. This procedure was repeated daily until the 5th day after ovulation or until the 20th day of the menstrual cycle for presumed anovulatory cycles. The time at which ovulation occurred was correlated with first signs of detumescence, both events occurring within a 24-hour period.     

A periodic dosing model of fetal alcohol syndrome in the pig-tailed macaque (Macaca nemestrina)

A nonhuman primate on a periodic ethanol dosing schedule should provide a model of fetal alcohol syndrome (FAS) most relevant to the majority of pregnant women who are “social drinkers” and can exercise reasonable control over their ethanol intake. In this pilot study, four pregnant pig-tailed macaques (Macaca nemestrina) received ethanol once a week from 40 days' gestation. Doses were 2.5 gm/kg for three moderate-dose animals (MDAs) and 4.1 gm/kg for one high-dose animal (HDA). Peak blood ethanol levels reached a mean of 240–256 mg/dl for the MDAs and averaged 379 mg/dl for the HDA. Peak acetaldehyde did not vary with dose. One MDA aborted after the first dose. The other three pregnancies were compared with eight to ten control pregnancies, and the infants' development over the first six months was compared with that of the control offspring. Nutritional status of the pregnant females was normal. The fetal heart rate response to maternal restraint was absent in the HDA. Gestational duration and simian Apgar scores were normal. All three infants were abnormally large, and two were also abnormally heavy, with body weight appropriate to skeletal size. Skeletal maturation, judged by ossification and tooth eruption, was not accelerated. The high-dose infant (HDI) was scaphocephalic, with an underdeveloped cranial base and midface, and its brain was small and dysplastic; its reflex, motor, and cognitive development were retarded. One moderate-dose infant (MDI) had some brain abnormalities; it was hyperkinetic and showed developmental retardation on several behavioral measures. The other MDI was normal. We conclude that the periodic model offers an effective means of investigating FAS in M. nemestrina. Furthermore, when nutrition is maintained, intermittent intake of ethanol by the pregnant primate does not necessarily reatard fetal growth.     

Factors influencing aggressive behavior and risk of trauma in the pigtail macaque (Macaca nemestrina).

Several experiments and surveys were conducted in a large colony of pigtail macaques (Macaca nemestrina) to determine some of the influences of spatial and social factors on aggressive behavior and risk of trauma. Female subjects exhibited more aggression when they had access to two-room suites than when they had access to single rooms. The frequency of aggressive interactions among females was positively related to the number of females per group. The presence of one or more males in groups inhibited aggressive interaction among females. Less aggression occurred among females in groups containing infants than in groups containing no infants. Provision of cover by introduction of concrete cylinders into rooms reduced aggression among members of stable groups. Subjects in newly-formed groups composed of unfamiliar animals sustained fewer injuries than did those in groups formed by merger of groups or subgroups of familiar animals.     

Growth and development of the term and premature pig-tailed macaque (Macaca nemestrina): Cardiovascular and respiratory changes during the first 3 weeks of life

Growth and development of the infant pigtailed macaque (Macaca nemestrina) over the first 3 weeks of life have been characterized by the variables of body weight, blood pressure, heart rate, ventilation, blood gas tensions, and lung mechanics. The effects of prematurity on postnatal developmental trends were assessed at gestational ages of 135–145 days (0.80 of term) and 150–155 days (0.91 of term). There was no indication that cesarean section, restraint, or instrumentation had any significant influence on the measurements. Gestational age at delivery had no effect on the minute ventilation per kilogram body weight, the hematocrit, or the heart rate; however, body weight, tidal volume, respiratory frequency, arterial gas tensions, blood pressure, and lung compliance did vary with gestational age at delivery. Postnatal maturational changes in these variables were similar between term and premature animals. The data for infant macaques and newborn humans were compared. The newborn macaque appears to be an excellent model of human developmental trends (and/or disease state) over the first 3 weeks of life, though some potentially important differences have been found.     

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

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

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

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

Sex hormones correlated with sex skin swelling and rectal temperature during the menstrual cycle of the pigtail macaque (Macaca nemestrina).

Daily measurement of serum luteinizing hormone, estradiol-17beta, and progesterone were made during the menstrual cycle in nine pigtail macaques (Macaca nemestrina). All data were normalized to the day of the luteinizing hormone peak. Serum estradiol-17beta increased from approximately 100 pg/ml during the early follicular phase to 442 +/- 156 pg/ml during the maximum midcycle concomitant with the luteinizing hormone peak, and a small increase in serum estradiol-17beta was observed during the luteal phase coincident with the progesterone peak. Serum progesterone values increased slightly at the time of the luteinizing hormone peak and increased from 0.2-0.3 ng/ml during the midfollicular phase to peak levels of 8.3 +/- 1.75 ng/ml 9 days after the luteinizing hormone surge. Serum luteinizing hormone remained low and relatively constant throughout the early and midcycle, then sharply increased approximately four-fold to peak values of 6.25 +/- 0.9 ng/ml. Sex skin swelling increased slowly during the follicular phase and declined slowly throughout the early luteal phase. Rectal temperature did not change significantly throughout the menstrual cycle. The similarity of plasma sex hormone changes during the menstrual cycle between women and the pigtail macaque suggested that this nonhuman primate should be a useful animal model for studying human reproduction.     

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.     

Mhc-DRB genes of the pigtail macaque (Macaca nemestrina): implications for the evolution of human DRB genes.

The DRB family of human class II major histocompatibility complex (Mhc) loci is unusual in that individuals differ in the number and combination of genes (haplotypes) they carry. Indications are that both the allelic and haplotype polymorphisms of the DRB loci predate speciation. Searching for the evolutionary origins of these polymorphisms, we have sequenced five DRB clones isolated from a cDNA library of a pigtail macaque (Macaca nemestrina) B lymphocyte line. The clones represent five different genes which we designate Mane-DRB*01-Mane-DRB*05. The genes appears to be approximately equidistant from each other, so that allelic relationships between them cannot be established on the basis of the sequence data alone. If positions coding for the peptide-binding region of the class II beta chains are eliminated from sequence comparisons, the Mane-DRB genes appear to be most closely related to the human (HLA) DRB1 genes of the DRw52 group. We interpret this finding to indicate that the ancestral gene of the DRw52 group of human DRB1 alleles separated from the rest of the HLA-DRB1 alleles before the separation of the Old World monkeys (Cercopithecoidea) from the apes (Hominoidea) in the early Oligocene. After this separation, the ancestral DRB1 gene of the DRw52 group duplicated in the Old World monkey lineage to give rise to genes at three loci at least, while in the ape lineage this gene may have remained single and diverged into a number of alleles instead. These findings suggest that some of the polymorphism currently present at the DRB1 locus is greater than 35 Myr old.     

Magnitude of sex differences in dichotomous ossification sequences of the hand and wrist

Among the dichotomous (present/absent:absent/present) ossinication sequences individually ascertained in 3059 boys and girls with at least one but not more than 27 ossification centers of the hand and wrist, 54 such sequences exhibit statistically-significant sex differences in frequency, 32 of them at the 1% confidence level or better. Analyzed by regions (rows and rays, epiphyses and round bones), ten centers, primarily distals and those of the first digit, account for the majority of the significant sex differences.     

Sex differences in the acquisition of communicative competence by pigtail macaques (Macaca nemestrina)

Previous study of captive pigtail monkeys (Macaca nemestrina) revealed that victims of an attack by a group member employed one of four acoustically different recruitment calls (Gouzoules&Gouzoules: Animal Behaviour 37:383–401, 1989). The calls appear to provide allies with information pertinent to decisions about fight intervention. Each call was associated with an agonistic context distinguished by the relative rank of the opponent and the severity of the attack. Monkeys younger than 3 years of age were significantly less likely to use a contextually appropriate call than were older animals and their calls tended to be acoustically less like the prototype for a given context. Analyses reported on here revealed that, among juveniles, females were more proficient than males in both the proper contextual use and the production of these calls. These findings suggest parallels with human sex differences in the development of communicative competence. The evolutionary origins for these sex differences in macaque vocal development may be based in the different life history patterns males and females exhibit.     

Attributes and validity of dominance hierarchy in the female pigtail macaque

A group of six unrelated female pigtail macaques,Macaca nemestrina, of the same age, was studied in captivity over a period of five years. The animals were observed under six different situations, following changes in the social composition of the group. The following social interactions were recorded: withdrawal, attack, threat, presentation, mount, and grooming. Although behavioural rates varied for each period, their distribution network was remarkably consistent. Each subject could be assigned a rank, which remained stable over the six periods. From an analysis of the number of dyads in which one of the two animal significantly performed both paired behaviours more than the other animal (external validity), behaviours clustered into two main groups: (1) attacks, threats, and withdrawals; and (2) mounts, presentations, and grooming. Quantitative methods were performed to standardize the degree in which linearity, stability, reciprocity, and idiosyncrasy of the interactions under study may account for social variability. When considering these properties, the behaviours clustered in the same two groups (“agonistic” and “affinitive”). A method to describe the dominance style ofMacaca nemestrina was proposed, which can easily be replicated for comparisons with females of other primate species and in different conditions.     

Feeding ecology of the long-tailed macaque(Macaca fascicularis) in Kalimantan Tengah,Indonesia

I studied long- tailed macaque (Macaca fascicularis)feeding behavior and ecology as part of a larger behavioral ecological study at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. I collected data on feeding behavior via scan sampling of all visible individuals in the focal group (approximately 800 observation hours). I established vegetational plots and monitored them monthly to determine food availability and abundance. I found long- tailed macaques to be primarily frugivorous;leaves, flowers, insects and bark provided the remainder of the diet. They used at least 33 plant species as food sources, but >60% of the diet was provided by only 5 species. Based on previous vegetational analyses, these tree species were among the highest in relative density. However, selection ratios for 19 food species indicate that 13 of them were selected more often than expected. Long- tailed macaques appear to be selective feeders but can exploit a variety of food sources during periods of food scarcity.     

Yawning,scratching, and protruded lips: Differential conditionability of natural acts in pigtail monkeys (Macaca nemestrina)

Food rewards were given contingent upon the performance of one of three natural responses in adult male pigtail macaques: scratching, yawning, and the facial expression “protruded lips.” Scratching rapidly increased in frequency when it was followed by food, as did variability in form of scratching and one form in particular, using the feet. The facial expression was resistant to the conditioning procedures. Yawning increased in frequency when followed by food, with extinction and reconditioning procedures confirming the establishment of the conditioned response. This is the first report of the conditioning of yawning in primates. Together, the results contribute to the literature on the differential conditionability of different classes of behavior, and suggest the possibility that macaques can voluntarily display “reflexive” acts for social goals.     

Daytime birth of a baby crested black macaque (Macaca nigra) in the wild

In mammals, which give birth to more or less dependent offspring, parturition usually takes place during the animals' resting period and in a secure environment. We report here the first direct and documented observation of a daytime birth of a wild baby crested black macaque, Macaca nigra, in the Tangkoko Batuangus Nature Reserve, North Sulawesi, Indonesia. We further consider the parturition time as a female reproductive strategy in a broader evolutionary framework.     

Helicobacter nemestrinae sp. nov., a spiral bacterium found in the stomach of a pigtailed macaque (Macaca nemestrina)

A new microaerophilic, spirally curved, rod-shaped bacterium was isolated from the gastric mucosa of a pigtailed macaque (Macaca nemestrina). The gram-negative cells of this bacterium are oxidase, catalase, and urease positive and strongly resemble Helicobacter pylori (Campylobacter pylori) cells. Like H. pylori, this organism does not metabolize glucose, does not reduce nitrate or produce indole, does not produce H2S from triple sugar iron agar, does not hydrolyze hippurate or esculin, and does not grow in the presence of 1% glycine, 1.5% salt, or 1% bile. Also like H. pylori, it is resistant to nalidixic acid and susceptible to cephalothin. However, unlike H. pylori, the colorless colonies are flat and have irregular edges. This organism has a unique cellular fatty acid composition, forming a new gas-liquid chromatography group, group K, and a distinctive DNA content (24 mol% guanine plus cytosine). It exhibits less than 10% DNA-DNA homology (as determined by the nylon filter blot method at 65 degrees C) with other members of the genus Helicobacter. Although the levels of DNA relatedness between previously described Helicobacter species and the new organism are low (less than 10%) and the difference in guanine-plus-cytosine content is large (24 versus 36 to 41 mol%), the genus Helicobacter is the only genus in which it is logical to include the organism at this time. We propose that our single strain represents a new species, Helicobacter nemestrinae, and we designate strain T81213-NTB (= ATCC 49396) as the type strain.     

Metric characteristics of the canine dental complex in prenatally androgenized female rhesus monkeys (Macaca mulatta).

Permanent maxillary canine teeth (C1) are appreciably larger in males than in females in most nonhominid Anthropoidea. Mandibular canines (C1) and mandibular first premolars (P3), against which C1 are sharpened in honing behavior, reflect commensurate sexual dimorphism. These three teeth constitute the canine dental complex. The canine complex crown metrics of seven mature genetically female rhesus Macaques, androgenized by prenatal exposure to testosterone propionate, were compared with a control sample (N = 12) for evidence of masculinization. The C1 and C1 were measured for clinical crown lengths (L) and mesiodistal and buccolingual widths. The functionally significant and highly dimorphic honing dimensions (HD), which approximate the honing surfaces of P3, were noted. In t-test comparisons, the C1 L and P3 HD in androgenized monkeys were significantly larger than those of the control group (P less than 0.05). Identical results were obtained with White's nonparametric ranking technique. Standardized lateral skull radiographs showing earlier dental formative stages were available for five of the seven animals, and these were compared with radiographs of control skulls. The developing C1 were longer and wider than in the controls. This was not reflected in the crown metrics of mature animals because of marked dental attrition. We concluded that androgens can masculinize the female rhesus canine complex, if given during critical periods of prenatal development. We hypothesize that genes encoding the male canine complex are normally activated by endogenous fetal androgens during such critical periods.     

Male intergroup mobility in a wild population of the Barbary macaque (Macaca sylvanus), Ghomaran rif mountains,Morocco

In this two-year study of a Barbary macaque population (n = 162) in the Ghomaran region of Morocco, 13 cases of males separated from their assumed natal groups were observed (nine visits of nonresident males to groups, two males isolated from groups as much as one day and one night, and two sets of snow tracks indicating males travel +7 km as isolates). Males left their assumed natal groups primarily in the mating season (12 cases), focused their interactions on estrous females of other groups, and were observed to copulate with these females in two cases. All males leaving their assumed natal groups were estimated to be between 5 and 8 years of age, with one exception (+ 15 years). It could not be determined whether males younger than 5 years moved between groups, or whether any males made permanent intergroup transfers. Regardless, the data from this study indicate that male intergroup mobility (and intergroup gene flow) was higher than has been previously assumed for this species. A prior theory that Barbary macaque groups are highly inbred, and that this is causally related to the evolution of male-infant care in this species, is not supported by the data of this study.