Operant conditioning of scratching in lemurs

An adult femaleLemur catta and an adult femaleEulemur fulvus were given edible rewards for scratching. Both subjects learned to scratch in order to obtain the rewards, showed diminished rates of scratching during periods of extinction, and learned to scratch preferentially with one foot when required. TheLemur catta subject was more responsive to the changing experimental conditions than theEulemur fulvus. The conditionability of scratching in primates does not appear to be directly related to the widespread occurrence of scratching in simian social contexts.     

Diurnal variation of common behaviors of pigtail monkeys (Macaca nemestrina)

Diurnal variation of eight common behaviors was studied in a social group of pigtail macaques (Macaca nemestrina). In agreement with previous work, all behaviors showed marked variation throughout the day, and differences between day and night levels were significant for most behaviors. Several significant inter-behavior correlations were found which suggested that common factors were major determinants of groups of behaviors. Significant correlations between separate diurnal cycles of sleep, grooming, and general activity demonstrated that these behaviors were among the most consistent with respect to diurnal cycles. The results point to the usefulness of diurnal studies in planning primate research designs, e.g., in controlling for variables associated with diurnal cycles.     

Social density and aggression in captive groups of pigtail monkeys (Macaca nemestrina)

A survey of aggressive behavior in 72 groups of pigtail monkeys (Macaca nemestrina) housed under identical spatial conditions revealed that frequency of contact aggression (grab, push, hit, bite) was directly related to social density. This result conforms with expectations of effects of crowding, but contrasts with previous work on responses to manipulation of spatial density. A similar paradoxical contrast between the effects of social density and spatial density has been documented in humans, and consequently development of a nonhuman primate model for study of crowding stress may be warranted. The choice of social density for captive nonhuman primate groups should be made with great care to avoid densities that result in destructive aggression.     

Age of menarche in pigtail monkeys (Macaca nemestrina): A cross-sectional survey of perineal tumescence

A four-month survey of perineal tumescence in 131 young female pigtail monkeys ($\text{Macaca nemestrina}$) revealed that most females had begun to swell by the time they were 3 years old. Those that had not begun to swell by that time were generally of lower weight than their peers. Those that tumesced before they were 3 years old tended to be heavier than their peers, but were not necessarily heavier than older, nonswelling females.     

A comparison of two timed-mating strategies for breeding pigtail monkeys. (Macaca nemestrina)

Pigtail monkeys (Macaca nemestrina) were time-mated using female perineal “sex skin” tumescence cyclicity as an indicator of ovulation time. The goal of these matings was production of infants of known gestational age for an investigation using a nonhuman primate model to study causes, correlates, and consequences of premature birth. Two breeding strategies were employed. The first involved allowing breeders constant access to one another for 72 hours at the time ovulation was predicted to occur from previous data on cyclicity of perineal tumescence. The second method limited exposure to two hours daily until perineal detumescence occurred. The second strategy has been considerably more effective than the first.     

Sex differences in use of a species-typical facial gesture by pigtail monkeys (Macaca nemestrina)

A species-typical gesture, the “jaw thrust”, was sequentially analyzed in a group of adultM. nemestrina. The major finding was a sex difference in apparent function with male jaw thrust sequences most likely to result in sexual behavior and female sequences most likely to terminate in agonistic behavior. Sex differences in the initiation and reception of jaw thrusts were also observed; they were most commonly initiated by males and directed toward females. Marked stereotypy of the behavioral sequences including jaw thrusts was observed: only a small proportion of the species’ behavioral repertoire was exhibited in temporal association with the gesture. Despite the striking nature of the gesture and the frequency with which it was exhibited, a majority of the signals had no overt social effect.     

Group formation of female pigtail macaques (Macaca nemestrina)

Human epidemiological studies have suggested that social variables can modulate the effects of stress on the immune system, and this concept has been gaining increasing attention with positive results emerging from empirical studies using nonhuman primates over the last two decades. Results from a previous study in rhesus monkeys suggested that receiving grooming positively affected recovery of T-helper and T-suppressor cells following the initial stress associated with group formation, and this co-varied with high dominance rank. Thus, the present study was undertaken in order to determine: (1) if the stress effect of formation could be replicated in another species and (2) if social behaviors or dominance rank, given that formation is a stressor, might independently correlate with physiological recovery from the stressor. Eight adult female pigtail macaques were moved from individual cages and simultaneously introduced into an outdoor enclosure along with an adult male, while eight weight-matched controls remained in individual caging. Behavioral data were collected during the introduction and over 4 weeks thereafter. Blood samples were collected prior to and at intervals for 4 weeks following formation. Compared to control subjects, the test subjects showed an increase in basal cortisol secretion (+28.9%) and a significant decrease in T-helper cells (-33.6%), T-suppressor cells (-30.8%), and B cells (-22.5%), while there was a significant increase in white blood cells (+29.5%) 24 hr following formation. When dominance rank and seven behavioral categories were analyzed, only the frequency of receiving grooming significantly predicted change, with animals who received a greater frequency of grooms showing a lesser negative percent change from baseline in the absolute number of T-helper cells 1 week following formation. The establishment of a dominance hierarchy, apparent within 1 week, was accomplished with no serious fighting and a complete absence of wounding or trauma, suggesting that psychosocial stress was responsible for the physiological changes observed. © 1996 Wiley-Liss, Inc.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

Luteolysis induced in pigtail monkeys (Macaca nemestrina) with prostaglandin f 2 alpha, ICI 80996 and ICI 81008.

Non-pregnant pigtail monkeys (M. nemestrina) were given ICI 80996 subcutaneously and ICI 81008 and PGF2alpha subcutaneously or intravaginally, once daily on days 20-30 inclusive, or two or three times on days 24 or 26 only. Doses of 50 mug/kg of ICI 80996, 100 mug/kg of ICI 81008 and approx. 1 mg/kg of PGF2alpha were used. In the majority of monkeys treated subcutaneously a rapid fall in circulating progesterone concentrations and earlier than normal menstrual bleeding occurred. When given per vaginam, ICI 81008 was as effective as when given subcutaneously, though PGF2alpha was less effective intravaginally than by the subcutaneous route.     

Teratogenic effects of retinoic acid in pigtail monkeys (Macaca nemestrina). I. General features.

Daily oral administration of 10 mg/kg retinoic acid to pregnant Macaca nemestrina monkeys on days 20 to 44 resulted in a high frequency of craniofacial and musculoskeletal malformations. Craniofacial defects including cleft palate and anomalies of the prinna were common as were ectrodactyly, kyphosis, and muscular-joint contractures. Transposition of the great vessels of the heart occurred in one animal and polycystic kidney and associated urogenital anomalies in another. Shorter treatment periods with similar or higher dosages were not teratogenic and were less fetocidal. Although only relatively long treatment courses were teratogenic, the defects that resulted were morphologically similar to those induced with retinoic acid or other vitamin A compounds in other animal orders.     

Taste difference thresholds for monosodium glutamate and sodium chloride in pigtail macaques (Macaca nemestrina) and spider monkeys (Ateles geoffroyi)

The purpose of this study was to determine taste difference thresholds for monosodium glutamate (MSG) and sodium chloride (NaCl) in pigtail macaques (Macaca nemestrina) and spider monkeys (Ateles geoffroyi). Using a two-bottle preference test of brief duration, three animals of each species were presented with four different reference concentrations of 50, 100, 200, and 400 mM of a tastant and tested for their ability to discriminate these from lower concentrations of the same tastant. The just noticeable differences (JNDs), expressed as Weber ratios (DeltaI/I), were found to range from 0.1 to 0.5 for MSG and 0.2 to 0.45 for NaCl in the pigtail macaques, with a significant tendency for higher Weber ratios with higher reference concentrations. In the spider monkeys, JNDs ranged from 0.15 to 0.4 for MSG and 0.1 to 0.25 for NaCl, with Weber ratios staying fairly constant across the reference concentrations tested. Thus, the JNDs were found to be generally similar in both species and to be at least as low as those found in humans for MSG and NaCl, as well as those found in spider monkeys for sucrose. The results support the assumption that both pigtail macaques and spider monkeys may use differences in perceived intensity of MSG and NaCl as a criterion for food selection.     

Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA

Mitochondrial DNA variation was surveyed in nine populations of the pigtail macaque (Macaca nemestrina), covering all three recognized subspecies in Southeast Asia. To do this, a 2,300 base pair fragment spanning the mitochondrial NAD 3 and NAD 4 genes and flanking tRNA subunits leucine and glycine was targeted for amplification and digested with a battery of 16 restriction endonucleases. Out of a total of 107 individuals, 32 unique haplotypes could be distinguished. Parsimony and neighbor-joining analyses grouped the haplotypes into five strongly supported assemblages representing China/Thailand, Malaysia, Sumatra, Borneo, and Siberut. These results indicate that the mainland and island mtDNA haplotypes are strictly and uniquely limited to the geographic ranges of the recognized morphological subspecies. Cladistic and neighbor-joining analyses indicate that inferred phylogenies of mtDNA haplotypes are congruent with subspecies designations. Furthermore, in support of morphological studies, results indicate that the Mentawai macaque is most likely not a distinct species but a subspecies of M. nemestrina. Am J Phys Anthropol 104:35–45, 1997. © 1997 Wiley-Liss, Inc.     

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.     

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.     

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.     

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.     

Response to social challenge in young bonnet (Macaca radiata) and pigtail (Macaca nemestrina) macaques is related to early maternal experiences

Previous experience affects how young primates respond to challenging social situations. The present retrospective study looked at one aspect of early experience, the quality of the mother-infant relationship, to determine its relationship to young bonnet and pigtail macaques' responses to two social challenges: temporary maternal separation at 5-6 months and permanent transfer to an unfamiliar peer group at 16-17 months. Relationship quality was measured quantitatively on 30 macaque mother-infant pairs with the Relationship Quality Index (RQI), the ratio of relative affiliation to relative agonism as previously applied to capuchin monkeys. Infants with high RQI values had amicable mother-infant relationships and infants with low RQI values had agonistic mother-infant relationships. Young monkeys with amicable and agonistic relationships showed consistent differences in behavior before, during, and after each social challenge, supporting the hypothesis that juveniles from amicable mother-infant relationships based on the RQI coped more effectively with social challenges than did juveniles from agonistic mother-infant relationships. Results suggest 1) characteristic amicability or agonism in early mother-offspring macaque relationships has the potential to influence offspring behavior in tense social contexts and 2) the RQI is useful as one of a coordinated suite of methods for studying the development of social skills.     

Luteolysis induced in pigtail monkeys (Macaca nemestrina) with prostaglandin F2α, ICI 80996 and ICI 81008

Non-pregnant pigtail monkeys (M. nemestrina) were given ICI 80996 subcutaneously and ICI 81008 and PGF_2α subcutaneously or intravaginally, once daily on days 20–30 inclusive, or two or three times on days 24 or 26 only. Doses of 50 μg/kg of ICI 80996, 100 μg/kg of ICI 81008 and approx. 1 mg/kg of PGF_2α were used.In the majority of monkeys treated subcutaneously a rapid fall in circulating progesterone concentrations and earlier than normal menstrual bleeding occurred. When given per vaginam, ICI 81008 was as effective as when given subcutaneously, though PGF_2α was less effective intravaginally than by the subcutaneous route.     

Luteolysis induced in pigtail monkeys (Macaca nemestrina) with prostaglandin F2α, ICI 80996 and ICI 81008

Non-pregnant pigtail monkeys (M. nemestrina) were given ICI 80996 subcutaneously and ICI 81008 and PGF_2α subcutaneously or intravaginally, once daily on days 20–30 inclusive, or two or three times on days 24 or 26 only. Doses of 50 μg/kg of ICI 80996, 100 μg/kg of ICI 81008 and approx. 1 mg/kg of PGF_2α were used.In the majority of monkeys treated subcutaneously a rapid fall in circulating progesterone concentrations and earlier than normal menstrual bleeding occurred. When given per vaginam, ICI 81008 was as effective as when given subcutaneously, though PGF_2α was less effective intravaginally than by the subcutaneous route.     

Species of the genus Macaca (Cercopithecidea, primates) as research subjects in modern biology and medicine

Members of the genus Macaca are the most commonly used animals in biomedical research on primates. Macaca monkeys are used most extensively (from 50% to 73% of the general file) in rapidly developing branches of medical primatology (pharmacology, endocrinology, ophthalmology, stomatology, and central nervous system pathology and physiology), i.e., in those sciences where monkeys are absolutely necessary and where they are used with great efficacy.