Environmental enrichment for captive stumptail macaques (Macaca arctoides)

Background  The behavior of animals is modified by captivity. Environmental enrichment (EE) is a program designed to enhance the welfare of confined animals by providing them with a more stimulating background. This is carried out by the implementation of a series of activities that encourages them to present behaviors typical of their species, as well as keeps them active. The aim of this study was the evaluation of the influence of the EE in the behavioral variables in a colony of 24 stumptail macaques ( Macaca arctoides ). Our hypothesis is that the application of this program will reduce aggression, stereotypes and coprophilia behaviors and, at the same time, will increase exploration and solitary play.
Methods  The behavioral frequency previous to EE was compared with that during EE implementation.
Results  Our results showed that aggression, coprophilia stereotypic behaviors and social play were significantly reduced during EE, whereas exploration was significantly enhanced. The response of the individuals according to gender was similar for both sexes.
Conclusions  Environmental enrichment programs are indispensable for captive animals' wellbeing as they reduce aggression and stress while providing animals both physical and cognitive entertainment.     

Formal biting in stumptailed macaques (Macaca arctoides)

Form and function of a specific kind of biting were studied in a captive group of stumptailed macaques (Macaca arctoides) composed of 1 adult male and 10 females. Behavior patterns were recorded with all occurrence and scan sampling techniques. Formal biting consisted of slowly gripping with teeth a part of the body of an apparently willing partner, most often the forearms, lips, or eyebrows. It may occur either following an agonistic interaction or outside the context of aggression. Such biting was directed from dominants towards subordinates, and appeared especially frequently between individuals having frequent agonistic interactions. It is concluded that this behavior represents a ritualized interaction expressing formal dominance between partners.     

Mirror-induced social facilitation in stumptailed macaques (Macaca arctoides)

Seven adult female stumptailed macaques (Macaca arctoides) were confronted alternately with their reflection in a mirror and with the mirror covered. The reflection elicited significantly more visual attention and social responding than the control stimulus, replicating previous findings. Mirror-image stimulation did not significantly affect the subjects' manipulation of unfamiliar objects, but it did increase bout-lengths of episodes of drinking from a bottle containing orange juice. Possible explanations for the ability of the mirror to induce social facilitation of drinking but not of object manipulation are discussed, along with possible underlying mechanisms. Mirror-induced social facilitation is further evidence that monkeys interpret their reflection as a conspecific.     

Some reproductive parameters of stumptailed macaques (Macaca arctoides)

Reproductive records kept from 1969 to 1981 were used to study menstrual cycles, pregnancies and births of eight colony-housed stumptailed macaques. The findings for annual distribution of births, pregnancy duration and infant sex ratio were consistent with previous reports. The interbirth interval after infant loss was significantly shortened from the interbirth interval when infants were maintained with their mothers. Vaginal bleeding during early lactation indicates that stumptails are not necessarily characterized by a prolonged period of postpartum amenorrhea. Complete copulation was observed prior to six months postpartum, but interbirth intervals indicate that conception did not occur prior to that time. Interbirth intervals tended to be shorter for dominant than for subordinate females and to lengthen as a function of increasing age.     

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.     

Responses to animal stimulus photographs in stumptailed macaques (Macaca arctoides)

Interest in their animate environment was studied in a captive group of 11 stumptailed macaques (Macaca arctoides). Subjects were shown projected photographic slides, most of which showed a single individual primate or non-primate. The measure of interest was the duration of viewing. Results showed that adult females exhibited more interest towards stumptailed macaques versus other macaques species, and towards adult females carrying infants versus adult females alone. Data concerning non-primates showed that subjects were especially interested by photographs of felids; this effect was partly due to the presence of two frontal and conspicuous eyes in felids.     

The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board

A new environmental enrichment device, termed a “foraging/grooming board,” was presented to 8 individually housed rhesus monkeys for the explicit purpose of reducing the level of aberrant behaviors manifested by these animals. The device, consisting of a piece of plexiglass covered with artificial fleece, had particles of food treats rubbed into it and was attached to the outside of each animal's home cage. All animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted. Most animals also groomed the fleece covering the board, utilizing the same motor patterns that would be directed toward grooming another monkey. These boards are inexpensive to construct and easy to sanitize, and do not require placing animal facility personnel at risk to maintain them.     

The effects of temporary removal of the alpha male on the behavior of subordinate male vervet monkeys

The effects of temporary removal of the alpha male on the behavior of subordinate adult male vervet monkeys were evaluated. Twelve subordinate males from six captive multimale, multifemale vervet monkey groups were observed in two conditions: when all group members were present and when the alpha male was temporarily removed from each group. In the absence of the alpha male, subordinate males initiated more affiliative behavior and increased the amount of time spent in proximity to females but their rates of aggression were unaltered. Increased affiliative behavior was selectively directed to high-ranking females and their offspring. Under removal conditions, subordinate male behavior did not resemble that of alpha males in intact conditions: they differed in their proximity to and affiliative behavior towards other group members. In the absence of the alpha male, females increased their aggression towards subordinate males. These observations suggest that the presence of alpha males strongly inhibits subordinate males' behavior. When the constraints of the alpha male's presence are removed, subordinate males rapidly engage in behavior that may enhance their likelihood of attaining high rank. In combination with prior studies, the data also indicate that the behaviors involved in the maintenance of high rank by alpha males differ from those subordinates use to acquire dominance. Finally the current study supports the view that aggression by female vervets may be highly influential in determining male ascendency to dominant rank.     

The structure of affiliative relations in a primate community: Allogrooming in stumptailed macaques (Macaca arctoides)

Social grooming in 19 adult stumptailed macaques (a dominant male and 18 females) was studied by focal sampling and scanning methods. Significant individual differences were found with respect to both active and passive grooming intensity, active grooming being a more variable parameter. Individual preferences in partner choice are very strong, but among the factors examined, age was the only one influencing these preferences. Neither social rank nor kinship were significant. The proportion of active and passive contacts shows marked individual differences. Yet, there is a positive association between performed and received grooming. The “extortion hypothesis” is not supported by our results: high-ranking individuals performed on the average more, and received relatively less grooming than low-ranking ones. High grooming performance of the dominants may secure group integrity in species with a “soft” dominance style.     

Female menstrual cyclicity and sexual behavior in stumptail Macaques (Macaca arctoides)

The sexual behavior and female reproductive cycles of a captive group of stumptail macaques (Macaca arctoides)were monitored during a 12-month period. The data, consisting of 303 ad libitummounts and copulations and 125 hr of focal-female testing, were analyzed by their frequency of occurrence during the three hormonal phases of the female menstrual cycle. Regularly cycling females exhibited statistically higher frequencies of all sexual behaviors compared to the amenorrheal controls. Contrary to previous reports which indicate no variation in sexual behavior throughout the reproductive cycle in this species, our data show marked increases in copulations during the periovulatory phase. Male dominance rank is associated with sexual behavior only at midcycle.     

The effect of inter-opponent distance on the occurrence of reconciliation in stumptail (Macaca arctoides) and rhesus macaques (Macaca mulatta)

Several studies have shown that affiliative contact between opponents increases after conflicts in a number of primate species. This study investigated the effect of inter-opponent distance on the occurence of reconciliation in stumptail and rhesus macaques. Both species were represented by multi-male, multi-female groups housed in large outdoor compounds. Ten-minute focal animal observations during post-conflict (PC) and matched control (MC) samples were collected in which affiliative interactions and the inter-opponent distance at the beginning of each sample were recorded. A total of 251 and 561 PC-MC opponent pairs were obtained for stumptail and rhesus macaques, respectively. Inter-opponent distance was smaller in PC than in MC observations for both stumptail and rhesus macaques. Conciliatory tendency varied as a function of the initial PC-MC inter-opponent distance. In particular, the closer opponents were in PC compared to MC periods, the more likely they were to reconcile. When the inter-opponent distance was the same in PC and MC periods the conciliatory tendency of both species was notably reduced. These findings have implications for the estimation of conciliatory tendency and its use in comparative studies.     

Social Contact Following Severe Aggression in Rhesus Macaques (Macaca mulatta): A New Test of the Consolation Hypothesis

Previous studies on macaque species revealed no evidence of consolation: affiliative contact between the loser of an aggressive interaction and a third party. However, typically, the researchers used short observation periods and latency to make first affiliative contact as a dependent measure. Based on social stress buffering literature, I predicted that by employing longer observation periods and percentage of time in affiliative contact as a dependent measure, I would be more likely to detect increases in affiliative contact following aggression. I observed adult female rhesus macaques for 1 hr after they received severe aggression and for 1 hr after some affiliative contact, and measured time spent in affiliative contact using instantaneous recording at 30-sec intervals. Contrary to prediction, victims of attack did not spend a greater percentage of time in affiliative contact postaggression as compared to postaffiliation. Subjects were also less likely to initiate contact with other individuals and were more likely to have contact with individuals that were dominant to their aggressor, following aggression. These results provide converging evidence that affiliative contact is not increased following aggression in macaques. I discuss the failure to bear out the predictions based on the social stress buffering literature in terms of rhesus social dynamics, the nature of aggression as a stressor, and possible mechanisms for the social stress buffering effect.     

Venipuncture and vaginal swabbing in an enclosure occupied by a mixed-sex group of stumptailed macaques (Macaca arctoides)

Procedures are described for vaginal swabbing and venipuncture in a gang-caged, mixed-sex group of stumptailed macaques. The design of the gang cages facilitated venipuncture and swabbing which were done without undue disturbance of the vivarium routine, without seriously stressing colony members, and without interfering with the monkeys' established social relationships.     

Endocrine changes in male stumptailed macaques (Macaca arctoides) as a response to odor stimulation with vaginal secretions

In mammalian species, social chemosignals are important in modulating endocrine reproductive functions. In nonhuman primates, previous studies have described a high frequency of mounting behavior by females in the follicular and periovulatory phases of the menstrual cycle. Stumptailed macaque females do not signal receptivity by means of sexual swellings, as do others macaques, therefore providing a good model in which to study chemical signaling of reproductive status. We exposed anesthetized stumptailed males to vaginal secretions of either late follicular or menses phase or to saline solution to determine the endocrine changes promoting male sexual behavior. In males exposed to follicular secretions, plasma testosterone concentrations were sustained up to 120 min after exposure. Such an effect was not observed in animals exposed to menses or saline odor sources. A luteinizing hormone surge, occurring 30 minutes after exposure to late follicular phase secretion swabs, preceded this sustained testosterone effect. The fact that late follicular scents induce sustained testosterone concentrations provides support to the idea that stumptailed males draw information concerning female reproductive status from the female's vaginal odor.     

The function of teeth chattering in male Barbary macaques (Macaca sylvanus)

Teeth chattering is seen in many primate species and has been proposed to have a range of social functions. This observational study tested specific hypotheses relating to the function of teeth chattering in a semi-free-ranging group of Barbary macaques, Macaca sylvanus. During focal watches of males, the outcome of male-male dyadic social interactions in which teeth chattering was present or absent was compared. Using these data, we tested the predictions of four hypotheses: teeth chattering functions as a signal of submission, appeasement, affiliation or reassurance. Support was found for all four hypotheses. In addition, in some contexts, an exchange of teeth chattering appeared to have a greater impact on the outcome of interactions than one male alone giving this signal. These findings suggest that teeth chattering serves an important role in coordinating the social interactions of male Barbary macaques.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

A statistical analysis of the social behavior of the male stumptail macaque (Macaca arctoides)

The social behavior of male stumptail macaques was analyzed in terms of behavioral sequences recorded during paired encounters in a large test cage. Recurrent patterns of behavioral sequences were sought and used to hypothesize the structure of motivational systems of social behavior as has been done previously for other species. In addition to traditional statistical analyses to determine which dyadic behavioral sequences were nonrandom, there were several methodological innovations. Instead of analyzing behavior as a single channel of communications, we analyzed three independent channels and considered their inter-correlations: 1) acts and postures; 2) vocalizations; and 3) facial expressions. Also, we analyzed not only within-animal behavioral sequences but between-animal sequences as well. Results were derived from 40 tests, most of which included vigorous agonistic and sexual interactions and a behavioral repertoire similar to that of adult male stumptail macaques observed by previous investigators. There were 30 acts and postures, eight facial expressions, and seven vocalizations that occurred more than five times. Many acts and postures occurred in nonrandom sequences, 43 such sequences within-animal and 40 between-animal. From these sequences and their correlations with specific vocalizations and facial expressions, it was possible to differentiate six categories of social behavior that may correspond to six different motivational systems: offense, defense, submission, groom and contact, male sexual behavior, and display. Both the frequency of behaviors in each category and the nature of the behavioral sequences were affected by the relative dominance of the two animals.     

Affiliative interference in mounts in a group of Tonkean macaques (Macaca tonkeana)

Affiliative interference in mounts was studied in a group of Tonkean macaques (Macaca tonkeana) living in semi-liberty. Over a 4-year period, 545 sexual and noncopulatory mounts accompanied by 367 instances of interference were recorded using behavior-dependent sampling. Interference by immature individuals was frequent and occurred mainly when the mother was the mountee. Interference by adult females was less common. Various behavior patterns were displayed in interference, mainly directed toward the mounter. Aggression by the latter was rare. However, interference occurred from further away with increasing age of the interfering individual. It is suggested that interference represents an attempt to be involved in interactions with influential individuals. Comparisons with other species support the hypothesis that the development of interference is related to species-typical social relationships and, in particular, that frequency and intensity of interference are determined by the tolerance of adult males.