Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

Effects of management methods,social organization,and physical space on primate behavior and health

The incidence of clinical treatment in a large colony of pigtailed macaques (Macaca, nemestrina) was studied retrospectively to assess the effectiveness of three sequential housing and management protocols. In the initial standard protocol, groups were housed in single rooms, with each room occupied by a different group after daily cleaning. In the experimental protocol, animals were housed in two-room suites dedicated exclusively to the resident group. This protocol was meant to reduce enteritis due to communication of Shigella flexneri across groups. Isolation of groups was coupled with the doubling of available space in an attempt to reduce stress. Under a final compromise protocol, a two-room suite was dedicated to each group, but the group occupied only one room at a time. The compromise protocol maximized isolation and reduced the available space to the level under the standard protocol. Thus, the study involved two main factors, the degree of group isolation and the amount and configuration of physical space available to each group. Under the experimental conditions enteritis increased, other communicable diseases did not decrease, and trauma from fighting increased by over 45% even though more space was available. Under the compromise conditions, trauma, enteritis, respiratory disorders, and inflammation all decreased markedly. Behavioral studies identified beneficial social behavior patterns associated with spatial reduction as the basis of the decrease in aggression, trauma, and disease under the compromise conditions.     

Effect of food preparation on feeding behavior of lion-tailed macaques

Ten group-living lion-tailed macaques (Macaca silenus), accustomed to receiving fruits and vegetable items of the diet in chopped form, were given these same foods in whole form to compare reactions to the non-nutritional properties of food. Contrary to common belief, the access of individuals to the different food items was not equalized through chopping into bite-sized morsels. Mean dietary diversity actually increased with presentation of whole foods, as did time spent feeding and total amount of food consumed. The widespread practice of chopping of food for captive primates has little to commend it in light of these findings.     

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.     

Leptin, adiposity, and testosterone in captive male macaques

Leptin is considered to act as a signal relating somatic energetic status to the reproductive system. However, the nature of that signal and its relationship with male reproductive function across nonhuman primate species are unclear. We suggest that species-specific differences in leptin physiology may be related to the degree of environmental variation and variation in the importance of energy stores for male reproduction. In order to test the role of seasonality in species differences among nonhuman primates, we compared leptin, testosterone, and body composition in male rhesus (n = 69) and pig-tailed (n = 43) macaques. Despite having larger abdominal fat deposits, the rhesus macaques did not exhibit significantly higher leptin levels (rhesus, 2.21 +/- 0.43 ng/ml; pig-tailed, 2.12 +/- 0.39 ng/ml). Both species showed increases in leptin across adolescent, subadult, and adult age-groups (P = 0.036 for rhesus; P = 0.0003 for pig-tailed by ANCOVA). Testosterone was not significantly associated with leptin in either the rhesus (r = 0.039; P = 0.754) or pig-tailed (r = 0.2862; P = 0.066) samples. Comparison of leptin levels across the two species using univariate modeling procedures showed no significant age-group by abdominal fat interaction. These findings suggest little difference in leptin production between these two closely related species, despite the difference in breeding seasonality.     

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

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

Social housing and pregnancy outcome in captive pigtailed macaques

We present a retrospective analysis of 30 years of breeding records from a colony of pigtailed macaques at the University of Washington's Regional Primate Research Center, specifically examining the effects on pregnancy outcome of sire presence, presence of other pregnant females, group stability, overall group size, and dam age and parity. Data on 2,040 pregnancies (1,890 live births) of socially housed pigtailed macaques (Macaca nemestrina) were obtained from the Washington Regional Primate Research Center's animal colony records from 1967 to 1996. Our results suggest that the presence of the sire and other pregnant females, fewer moves, and lower parity increases the probability of a viable birth. In viable and nonviable births, gestation length was positively related to contact with the sire and other pregnant females, number of moves, and dam age. Once the effect of gestational age was taken into account, birthweight increased with increasing parity and decreased with dam age. Clinical treatment of the dam decreased as sire presence and group size increased and number of moves decreased. The length of treatment was dependent on the number of moves experienced by the dam, with more moves associated with longer treatments. Sire presence was the single most important factor in nearly all measures of reproductive outcome. Am. J. Primatol. 47:153–163, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

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.     

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.     

Ossification in the hand and foot of the pigtail macaque (Macaca nemestrina). II. Order of appearance of centers and variability in sequence

The order of appearance of the carpals, tarsals and secondary epiphyseal centers in the hand-wrist and foot-ankle regions of the fetal and infant pigtail macaque (Macaca nemestrina) was reconstructed using a cross-sectional sample of 127 animals and a longitudinal one of 14 animals. Comparison of the most common sequence in the monkey with that described in the human studies showed major interspecific differences in the order of appearance of several groups of centers, particularly those involving the thumb and great toe. The monkey displays a degree of sequence variability equivalent to that documented by the human longitudinal data, with certain centers markedly variable in timing and/or order of appearance. The evidence from related animals suggests a strong genetic component underlying some of the variable sequences observed, as has been reported in the human studies. The demonstrated variability in both timing and sequence precludes the use of specific centers in the determination of gestational age in fetuses of unknown conception date.     

Interactions between lar gibbons and pig-tailed macaques at fruit sources

Interactions are reported between white-handed gibbons (Hylobates lar) and pig-tailed macaques (Macaca nemestrina) in Khao Yai National Park, Thailand, in which gibbons selected ripe fruit from sources before macaques arrived on 4 occasions during June and July of 1989. The macaques foraged near gibbons or from shared fruit sources during 13% of gibbon observation time. Gibbons made their presence known in fruit trees when macaques approached on 3 occasions and macaques did not enter fruit trees occupied by gibbons. An aggressive interaction is reported in which a single white-handed gibbon vigorously excluded 22–28 macaques from a rare and valuable fruit tree (Sandoricum koetjape). The observations suggest that exploitative and interference competition may exist between these species.     

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.     

Food distribution,dominance, and aggressive behaviors in bonnet macaques

Resource availability or distribution may affect interindividual competition in species such as primates, which forage in social groups, and several field studies suggest that dominance status predicts access to restricted food sources. Increased competition due to restricted resources may result in the intensification of aggressive behaviors. The study reported here examines the impact of manipulation of the distribution of food resources in a laboratory-housed group of bonnet macaques to assess the impact of distribution on aggressive behaviors. Food was restricted to a space which allowed access to only one or two individuals at a time or was dispersed throughout the living enclosure to allow universal access in alternating periods. During periods of clumped distribution, the monkeys obtained access to the food in order of their dominance status in the group. In addition, overall levels of aggressive behaviors increased, submissive behavior increased, and play decreased during periods of clumped distribution of food. These results confirm the findings from field studies indicating increases in agonism with restriction of food resources. These findings also have implications for primate colony management, in terms of developing strategies for minimizing intragroup aggression in captive groups.     

Determining overweight and underweight with a new weight‐for‐height index in captive group‐housed macaques

Housing primates in naturalistic groups provides social benefits relative to solitary housing. However, food intake may vary across individuals, possibly resulting in overweight and underweight individuals. Information on relative adiposity (the amount of fat tissue relative to body weight) is needed to monitor overweight and underweight of group‐housed individuals. However, the upper and lower relative adiposity boundaries are currently only known for macaques living solitarily in small cages. We determined the best measure of relative adiposity and explored the boundaries of overweight and underweight to investigate their incidence in group‐housed adult male and female rhesus macaques and long‐tailed macaques living in spacious enclosures at the Biomedical Primate Research Centre (BPRC), the Netherlands. During yearly health checks different relative adiposity measures were obtained. For long‐tailed macaques, comparable data on founder and wild animals were also available. Weight‐for‐height indices (WHI) with height to the power of 3.0 (WHI3.0) for rhesus macaques and 2.7 (WHI2.7) for long‐tailed macaques were optimally independent of height and were highly correlated with other relative adiposity measures. The boundary for overweight was similar in group‐housed and solitary‐housed macaques. A lower boundary for underweight, based on 2% body fat similar to wild primates, gave a better estimate for underweight in group‐housed macaques. We propose that for captive group‐housed rhesus macaques relative adiposity should range between 42 and 67 (WHI3.0) and for long‐tailed macaques between 39 and 62 (WHI2.7). The majority of group‐housed macaques in this facility have a normal relative adiposity, a considerable proportion (17–23%) is overweight, and a few (0–3%) are underweight.     

Food puzzle for singly caged primates

To enhance environmental complexity for singly caged pigtailed macaques (Macaca nemestrina), we designed a food puzzle to promote foraging. The puzzles, made of clear plastic tubing and loaded with peanuts in the shell, were suspended from linked chains and attached to the fronts of the cages. Animals manipulated the puzzles by reaching through a cage opening. Upon presentation of loaded puzzles, most animals attempted to remove the peanuts. More peanuts were removed within an hour after the puzzle was loaded than at any other time during the day. Young adult animals showed no sex differences in number of peanuts removed and were more proficient than middle-aged animals in removing peanuts during the first hour of testing. Middle-aged females were more proficient than middle-aged males. The food puzzle enhanced the animals' cage environment by providing a goal-oriented activity that they could control. © 1992 Wiley-Liss, Inc.     

Climbing test to measure gross motor development in monkeys

This report describes an apparatus, protocol, and coding procedure to quantify gross motor skills in infant Macaca nemestrina, and presents data obtained from this system. The apparatus consists of a 1.8-m-tall Plexiglas tube extending from the top of a standard stainless steel cage. Animals climb the tube to reach a food reward. Measures of climbing ability included time and number of contacts with the tube. Data were collected on 336 climbs to the highest level (1.5 m) on eight normal infants. Three subjects began training at two months of age, three began at three months, and two began at four months. Exploratory data analysis revealed that Time Up was the best measure due to low variability between and within subjects, high motivation of the subjects to reach the food reward, and ease of measurement. Though this pilot study is based upon a limited sample size, two-month-olds were consistently slower and more variable than the three- and four-month-olds. Relatively few sessions are required to train the subject and obtain measures of a subject's motor ability. The advantages of the climbing tube are that it is inexpensive to operate, provides a large amount of data, and appeals to the subject's natural propensity to climb. © 1995 Wiley-Liss, Inc.     

Chromobacterium violaceum infections in 13 non-human primates

Background Recently, an Indian‐origin macaque was found dead and Chromobacterium violaceum was isolated from the skin wound, and hepatic and pulmonary abscesses. Methods By searching the database, a total of thirteen cases of C. violaceum infection in pigtail macaques (n = 8), rhesus macaques (n = 4), and one baboon were identified from 2001 to 2010 at Tulane National Primate Research Center. Medical records were reviewed for breed, sex, age, clinical findings, treatment, outcome, bacteriology, and gross and histological findings. Results Seven pigtail macaques and one Indian‐origin rhesus macaque died of chromobacterial septicemia. All chromobacterial septicemic pigtail macaques were adult with higher incidence in female. Hepatic abscess and thrombosis were typical findings along with pulmonary abscess and thrombosis, renal venous thromboembolism, and necrosuppurative pleuritis, peritonitis, splenitis, myocarditis, pericarditis, and meningoencephalitis. Skin wound, uterine infection, and oral and respiratory exposure were considered the points of entry for these animals. Conclusions This represents the first report of chromobacteriosis in pigtail, rhesus macaque, and baboon. Our experience suggests that chromobacterial infections may be more common in non‐human primates than previously recognized.