Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta)

Due to primate adaptations for sociality, captive rhesus macaques have optimal welfare and utility as a biomedical model when they can be maintained in outdoor social groups. As a despotic species; however, aggression can result in costly injuries and may result in temporary or permanent removal of specific individuals from social housing. Enrichment items, such as toys, climbing structures, and foraging material, are employed to keep captive animals occupied. We hypothesized that produce enrichment that requires more processing to extract may reduce socially‐derived injuries by keeping animals occupied. We tested the effects of additional weekly produce (corn‐in‐husk, whole melon, or whole squash) on trauma incidence in an outdoor social group of rhesus macaques across two distinct seasons (mating and birthing seasons) at the California National Primate Research Center. Aggression and status behavioral data, food resource use and proximity, and trauma incidence were collected over two 16‐week periods, with eight control and treatment conditions alternating biweekly. Mixed‐effects regression modeling was used to determine the best predictors of trauma risk and severe aggression at the group level and at an individual level. We found that food resource use was an important predictor of trauma risk at both group and individual levels; greater use of food resources reduced trauma risk. Produce enrichment did not; however, reduce severe aggression. We suggest that other captive social groups of rhesus macaques with high levels of trauma may benefit from supplemental produce enrichment that increases animal engagement with food resources.     

A behavioral profile for stumptail macaques (Macaca arctoides)

Behavioral observations made on a group of 15 stumptail macaques living in a seminatural environment are used to delineate an activity profile for the species which embraces numerous locomotor, self-directed, environment-directed and social behaviors. Data indicating that certain animals direct or receive particular behaviors at markedly different rates than the rest of the group are noted. The data from 39,000 10-sec observational samples are used to construct a detailed behavioral time-budget for the group. The budget takes into account the co-occurrence rates of the most frequently observed behaviors with each other and with the other behaviors recorded. The activity profile constructed in this way is compared with the results of four other studies which estimate daily behavioral rates for the species. Environmental, social group composition and sampling-technique variables are considered for their probable effects upon the behavioral rates reported in both the present and the compared studies. A detailed comparison of data from the different studies permits the estimate of a species-typical rate for each of the behavioral patterns reported and commented upon. The estimated rates, expressed as a range of values indicating the percentage of time that an average group member dedicates to various behaviors, should be valid in a wide variety of environments.     

Video-induced yawning in stumptail macaques (Macaca arctoides)

This study reports the first experimental exploration of possible contagious yawning in monkeys. Twenty-two stumptail macaques (Macaca arctoides) were presented with video clips of either yawns or control mouth movements by conspecifics. At a group level, monkeys yawned significantly more often during and just after the yawn tape than the control tape. Supplementary analysis revealed that the yawn tape also elicited significantly more self-directed scratching responses than the control tape, which suggests that yawning might have been caused by tension arising from viewing the yawn tape. Understanding to what extent the observed effect resembles contagious yawning as found in humans and chimpanzees requires more detailed experimentation.     

Non-seasonal breeding pattterns in stumptail macaques (Macaca arctoides)

This paper summarizes published reports of breeding patterns across the genusMacaca. Patterns range from strictly seasonal to non-seasonal. Data on sexual behavior and birth patterns are presented which confirm previous reports of non-seasonality forMacaca arctoides. In a captive colony, 63 births were recorded, and individuals were born during every month of the year. Heterosexual mounting activity was recorded over a two-year period and occurred during every month of that period. It is clear thatM. arctoides does not exhibit the seasonal cyclicity observed in some other macaque species.     

Female-infant interactions among free-ranging stumptail macaques (Macaca arctoides)

The friendly and aggressive behaviors directed by females other than the mother to the troop's infants were recorded during a six-month long study of stumptail macaques living on an island. A great deal of friendly contacts were directed by the females toward the troop's infants. Juvenile females interacted with infants mainly through social play while adult females directed passive contacts (e.g., touch-hand) to them. While the adult females displayed more care contacts toward male infants the juvenile females preferred the female infants. The social position of the infant's mother in the troop and the attention it received from the males regulated the caring behavior an infant received from the females.     

The effects of temporary cover on the behavior of socially housed stumptailed macaques (Macaca arctoides)

To examine the effects of the provision of temporary cover on the behavior of stumptailed macaques (Macaca arctoides), a single group of 26 animals was observed during 25 testing periods over 7.5 months. During each testing period, the group was observed under two conditions. In the Cover condition, two solid temporary walls 9.6 m in length, were erected within the animals' living compound. In the No-Cover condition, the wall materials were stacked against one solid exterior wall of the compound. The provision of cover significantly reduced the levels of contact aggression, proximity between animals, and locomotion, and reduced the ability of the dominant male to monopolize copulations. It did not effect other measures of affiliation. Inconsistencies between these results and those of other published studies suggest that, while cover can have a significant influence on some kinds of social behavior in some situations, generalizations about the benefits of providing cover to captive animals may be premature.     

Blood variables in adult stumptail macaques (Macaca arctoides) living in a captive group; annual variability

Monthly blood samples were collected for more than two years from adult stumptail macaques living in a large captive group. The social organization, feeding pattern, and food composition were stable throughout the study period. No seasonal variability was observed for any of the 30 blood variables studied. It appeared that for each variable, within-animal variance was small relative to between-animal variance. A table of means and reference ranges is presented and discussed.     

Social communication among captive stump-tailed macaques (Macaca arctoides)

I compared the frequency of occurrence, contextual usage, and meaning of some of the most prominent gestural signals in stump-tailed macaques. I recorded the occurrence of 15 visual and tactile behavior patterns in a multimale multifemale captive group of stump-tailed macaques with the behavior sampling method in 100 hr of observation and analyzed the data via factor analysis and analyis of variance. The hindquarter presentation was the most frequent gesture. It was displayed by subordinates to appease dominants even in the absence of impending risk of aggression. Bared-teeth, lip-smack, teeth-chatter, and present-arm are submissive signals as well, but they differ from the presentation and from one another in their contextual usage. Nonthrusting mount, hip-touch, hip-clasp, and genital manipulation are directed down the hierarchy and appear to reflect dominance, reassurance, protection, or bonding. Mock-bite is a ritualized aggressive behavior pattern, often used to resolve uncertain dominance relationships. Ventroventral embrace occurs as a female bonding pattern. Overall, most gestural signals in stump-tailed macaques relate to dominance and submission and, to a lesser extent, social bonding.     

Menstrual-cycle phase and sexual behavior in semi-free-ranging stumptail macaques (Macaca arctoides)

The sexual behavior and female reproductive cycles of a group of island-dwelling stumptail macaques (Macaca arctoides)were monitored over a 6-month period, yielding 530 observation hr and 268 copulations. Compared to nondominant males, the dominant male copulated at a relatively high rate throughout the cycle, but largely with one high-ranking female. The non-dominant males copulated most frequently at midcycle. Female presenting was highest at midcycle, but only to the dominant male. Cross-study discrepancies may be due to different observation methods and restricted environmental conditions that mask female-initiated sexual behavior. The more naturalistic setting of this study allowed for a fuller expression of proceptivity. Contrary to some previous conclusions, present findings suggest that both hormonal and socioenvironmental factors influence the patterns of sexual behavior found in stumptail macaque colonies.     

Continued copulation of ovariectomized adrenal-suppressed stumptail macaques (Macaca arctoides).

Female stumptail macaques continue to copulate at moderate to high levels for years after gonadectomy. This study examined the extent to which sexual behavior of ovariectomized stumptail females was maintained by steroids of adrenal origin, and second, considered the possibility that ovarian fragments might have been left in situ following surgery. Daily injections of 0.1 mg of dexamethasone sodium phosphate suppressed serum cortisol, estradiol, and testosterone by at least 85% in three of four ovariectomized females, but dihydrotestosterone was suppressed by only 50 to 70%. The fourth female showed maximal suppression of cortisol but maintained much higher levels of the other steroids, in particular estradiol, and therefore it was strongly suspected that this animal had an ovarian fragment.Within the limits to which sex steroids were depressed with dexamethasone, no correlation was found between steroid levels and sexual performance. Ejaculatory frequencies and measures of attractivity, proceptivity, and receptivity collected during heterosexual pair tests remained unaffected in all four females during 4 weeks of dexamethasone treatment. Thus it was concluded that the maintenance of copulatory activity after ovariectomy in this species was largely due to nonsteroidal mechanisms.     

Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta)

Captive groups of primates often exhibit higher rates of aggression than wild, free-ranging groups. It is important to determine which factors influence aggression in captivity because aggression, particularly intense aggression, can be harmful to animal health and well-being. In this study, we investigated the effect of ground substrate as well as season, rank, age, and group size on rates of agonistic interactions per female in seven captive groups of rhesus macaques (n = 70 females, 1,723 focal samples) at the California National Primate Research Center. Agonistic interactions were divided into three categories: displacements, mild aggression, and intense aggression. Females living in enclosures with gravel substrate were 1.7 times more likely to be involved in intense aggression (e.g. chases and physical contact) than females living in enclosures with grass (Poisson regression model: P < 0.001). High-ranking females were at least 1.3 times more likely to be involved in mild (e.g. threats and lunges) aggression than lower-ranking females (low rank: P = 0.03; mid rank: P = 0.001). Females of all ranks were 1.5-1.9 times more likely to be involved in both intense and mild aggression during the breeding season than other seasons. Age and group size did not affect rates of mild or intense aggression. These findings indicate that although some aggression appears to be natural and unavoidable, i.e. aggression during the breeding season, the well-being of captive macaques can be improved by developing grass substrate in outdoor enclosures.     

Interaction patterns of two newly formed groups of stumptail macaques (Macaca arctoides)

Shortly after two groups of stumptail macaques were formed, their individual and social behavior was observed. Similar overall behavior of the two groups arose from different interaction patterns within the groups. Hierarchical stabilities and instabilities were related to selective affilliation patterns. The main instabilities were found at the top of the hierarchy of one group and in the middle of the other. The roots of later changes in group structure were displayed in individual association preferences.     

Contrafreeloading in grizzly bears: implications for captive foraging enrichment

Although traditional feeding regimens for captive animals were focused on meeting physiological needs to assure good health, more recently emphasis has also been placed on non‐nutritive aspects of feeding. The provision of foraging materials to diversify feeding behavior is a common practice in zoos but selective consumption of foraging enrichment items over more balanced “chow” diets could lead to nutrient imbalance. One alternative is to provide balanced diets in a contrafreeloading paradigm. Contrafreeloading occurs when animals choose resources that require effort to exploit when identical resources are freely available. To investigate contrafreeloading and its potential as a theoretical foundation for foraging enrichment, we conducted two experiments with captive grizzly bears (Ursus arctos horribilis). In Experiment 1, bears were presented with five foraging choices simultaneously: apples, apples in ice, salmon, salmon in ice, and plain ice under two levels of food restriction. Two measures of contrafreeloading were considered: weight of earned food consumed and time spent working for earned food. More free than earned food was eaten, with only two bears consuming food extracted from ice, but all bears spent more time manipulating ice containing salmon or apples than plain ice regardless of level of food restriction. In Experiment 2, food‐restricted bears were presented with three foraging choices simultaneously: apples, apples inside a box, and an empty box. Although they ate more free than earned food, five bears consumed food from boxes and all spent more time manipulating boxes containing apples than empty boxes. Our findings support the provision of contrafreeloading opportunities as a foraging enrichment strategy for captive wildlife. Zoo Biol 29:484–502, 2010. © 2009 Wiley‐Liss, Inc.     

Copulatory behavior in a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico

This paper presents copulatory data gathered on a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico. The study found evidence for seasonal clumping of matings, with the peak in the month of February, and that matings are more common in the afternoon, when measuring diurnal changes. It also found that males require an average of one and a half mounts before ejaculating, and mating among females is distributed unequally, when the measurement is between those females that mated. Furthermore, male dominance rank and male-female affiliation are both positively correlated with mating frequency. Variations between this study and captive studies are minimal. The variances that do occur may be explained by differences in the research settings or the individual differences in the subjects' behavior across studies.     

Return-benefit spite hypothesis: An explanation for sexual interference in stumptail macaques (Macaca arctoides)

Sexual interference behavior (the phenomenon of intervening with the matings of others) appears selfish in that its primary function seems to be that of improving one's reproductive fitness relative to others. In stumptail macaques (Macaca arctoides), interference may be spiteful, and may contribute to the receipt of a return benefit. This is the focus of this paper. The subjects were 58 stumptail macaques in a single group with seven matrilines. They were free-ranging, habituated to human observation, and lived on the island of Tanaxpillo at Lake Catemaco in southeastern Mexico. During the study, tie durations (the periods where male and female genitalia remain connected following ejaculation) were significantly altered overall, being longer, on average, during matings with sexual interference, opposed to those without interference. When matings occurring in succession were divided in half, ties were significantly longer during the second half than the first half. Also, although the difference was not statistically significant, the average number of mounts required by males to reach ejaculation was greater during matings with interference than without interference. Such apparent social stress may reduce the fertility of the mating pair at some cost to the interferer. Some individuals that interfered also used alternative mating tactics. These matings were 27% of the total, and they received interference less often than normal matings. When alternative matings were interfered with, they received significantly less interference: alternative matings received nearly eight times less interference than normal matings. The average tie duration for alternative matings without interference was also significantly less than the average tie for normal matings with interference. Alternative mating tactics appear to elicit less social stress; this may contribute to increased reproductive fitness for individuals that practice both alternative mating and sexual interference, if the latter produces a return benefit.     

Changes in the social structure of two groups of stumptail macaques (Macaca arctoides)

Two previously studied groups of stumptail macaques were restudied to investigate stabilities and instabilities within group structures. Frequency data for nonsocial and dyad behaviors were collected. While there was considerable group stability, several important changes occurred. The most noteworthy group changes were in grooming and playing. Individual changes centered upon females. The first and fourth ranking females of one group switched dominance positions. The roots of this reversal were minimally reflected by aggressive and submissive interactions, and more fully exposed by quiet association patterns such as grooming, huddling, and sitting together. Increased frequencies of huddling, touching, and approaching indicated that the lowest ranking female of each group moved closer to other group members. There was no hint of this change in agonistic interactions.     

Patterns of wounding in stumptail macaques (macaca arctoides)

A three-year study of the patterns of wounding in a group of stumptail macaques (Macaca arctoides) was conducted at the Yerkes Regional Primate Research Center Field Station. Wounds were classified as punctures, lacerations or abrasions. Data were analyzed to determine if patterns of wounding vary by age/sex class, body part or wound type. Results indicate that adult males receive significantly more total wounds than expected, based on their total time spent in the group. Adult males also receive more serious wounds than other age/sex classes. Low-ranking animals are wounded more often than high-ranking individuals. Moreover, the location of wounds within each age/sex class is non-random. Adult males receive a disproportionate number of wounds on the forequarters, but adult and immature females are wounded disproportionately on the hindquarters. Finally, age/sex classes differ in the number of wounds on individual body parts. Adult males receive more wounds on the head, arms and hands than other age/sex classes, but adult and immature females receive more wounds on the feet than other age/sex classes. These results demonstrate that wounding patterns are clearly non-random and depend on a variety of factors such as age, sex and dominance rank.     

Establishment of a free-ranging colony of stumptail macaques (Macaca arctoides): Social relations I

Data on the social behaviour of a free-ranging troop of Stumptail macaques are reported for a period starting of August 15th to November 7th of 1974. Positive interactions take a greater part in the daily life of the troop than negative interactions. Individuals order themselves in an essentially linear dominance hierarchy and offspring rank immediately below their mother. Agonism and displacement are good predictors of dominance rank. Dominant individuals are a strong source of attraction for subordinates and the alpha male is a powerful social magnet for immatures. Grooming was found to be correlated with dominance rank and individuals holding adjacent ranks tend to interact positively with one another. To gain access to dominant females, subordinates direct a great deal of positive behaviour to the female’s youngest offspring. As social distance decreases the selection of a social partner becomes more strict and tends toward adjacency. However, factors such as motherhood, genealogical ties, and special relationships with non adjacent individuals, can override the tendency. The direction and quantity of male-care displayed by the adult male and by juvenile males toward younger individuals was found to be influenced by the troop’s dominance patterns. Sex differences were found to exist in male-care received and a negative association was found with the age of the receiver. Adult females are the main regulators of social relations and their rank and friendships provide their offspring with the social format, before puberty, in which they develop socially. The alpha male is the group protector, the performer of policing, an important element in the immatures’ social development, and a powerful source of attraction for all troop members.     

Testosterone, testis size, seasonality, and behavior in group-living stumptail macaques (Macaca arctoides)

During a 28-month period, data were collected on physiological parameters and sociosexual behavior of 13 adult male members of a large mixed-sex group of stumptail macaques living in an outdoor cage. Monthly measurements of plasma testosterone, testis size, and body weight revealed no systematic seasonality. Seasonal variations did occur in branch shaking and grooming (both with low rates in winter), but not in other behaviors studied (copulation, masturbation, aggression). Dominance ranks were stable throughout the study period and were not significantly correlated with mean testosterone levels. Temporal fluctuations in behavioral frequencies did not parallel testosterone fluctuations. Interindividual differences in behavioral frequencies were often correlated with dominance rank, but not with testosterone levels.