Mirror guided behavior in Japanese monkeys (Macaca fuscata fuscata)

Two male Japanese monkeys were trained to use a mirror to reach an object that could not be seen directly. Training to use a mirror in this way proceeded, step-by-step, from reaching a piece of apple to key-tracking. In Experiment 1 the monkeys were trained to use the mirror to locate a desired object, a piece of apple in a box facing the mirror, which could be seen only by looking into the mirror. The apple, once located, however, could be grasped without further reference to the mirror. This behavior is referred to as mirror mediated object discrimination. In subsequent experiments the monkeys could not reach the goal object except by observing it and his hand movement in the mirror. In Experiment 2 the target was a piece of apple visible in the mirror, in Experiment 3 an illuminated key and in Experiment 4 a series of keys which were illuminated sequentially. Mirror guided behavior such as shown in Experiment 2, 3, and 4 has not previously been demonstrated in monkeys.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

Mirror mediated object discrimination and self-directed behavior in a female gorilla

Mirror mediated object discrimination was investigated in a captive female, human-reared, western lowland gorilla (Gorilla gorilla gorilla) approximately 26 years of age. The gorilla was trained to find a stimulus that was only visible by use of the mirror. The gorilla could not reach the goal object except by observing it in the mirror and her hand movement was not visible through the mirror. Further, it was hypothesized that this mirror mediated object discrimination would enhance the probability of self-directed behavior.Gallup’s (1970) marking paradigm, excluding the use of general anesthesia, was utilized in assessing self-directed behavior. Mirror-gazing, face-directed, and mark-directed behavior with a mirror were compared before versus after discrimination mirror training. The results supported the hypotheses that gorillas are capable of mirror mediated object discrimination and that mirror training involving a discrimination task would facilitate self-directed behavior.     

Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella)

The purpose of this study was to examine the hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Two experiments were conducted. In Experiment 1 capuchins were presented with an apparatus designed to accommodate the use of probing tools. In Experiment 2 the same capuchins were presented with sets of nesting containers. Five of the ten subjects used probing tools and seven subjects placed objects in the containers. The capuchins' behavior reflected three hierarchically organized combinatorial patterns displayed by chimpanzees and human infants. Although the capuchins sometimes displayed the two more complex patterns (“pot” and “subassembly”), their combinatorial behavior was dominated by the simplest pattern (“pairing”). In this regard capuchins may not attain the same grammar of manipulative action that has been reported for chimpanzees and young human children. © 1994 Wiley-Liss, Inc.     

Macaques (Macaca nemestrina) recognize when they are being imitated

This study investigated whether monkeys recognize when a human experimenter imitates their actions towards an object. Two experimenters faced 10 pigtailed macaques, who were given access to an interesting object. One experimenter imitated the monkeys' object-directed actions, the other performed temporally contingent but structurally different object-directed actions. Results show a significant visual preference for the imitator during manual object manipulations, but not mouthing actions. We argue that the ability to match actions could be based on both visual-visual and kinaesthetic-visual matching skills, and that mirror neurons, which have both visual and motor properties, could serve as a neural basis for recognizing imitation. However, imitation recognition as assessed by visual preference does not necessarily imply the capacity to attribute imitative intentionality to the imitator. The monkeys might implicitly recognize when they are being imitated without deeper insight into the mental processes of others.     

An analysis of dyadic interactions of male Japanese monkeys (Macaca fuscata fuscata) in a cage-room observation

This is a laboratory observation (Home-cage and observation room) for individual and social behavior of four male Japanese monkeys. The monkeys were placed in a dyadic and trio situation with the purpose to investigate the relationships between aggressive and affinitive factors which regulated their social behaviour. Total amounts of attacks and receiving groom showed a consistent order for four monkeys through the pairwise conditions, which was presumed to indicate a dominance order. Grooming and mounting behavior, however, were influenced by the particular dyadic interactions, probably social attraction, rather than dominance order itself. The presence of the third animal facilitated such a social preference between animals positioned closely in the rank order as well as elicited aggression from the dominant animals.     

Effect of others' attentional states on vocalizations in Japanese monkeys (Macaca fuscata)

We investigated the effects of other's attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter's body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly.     

Discrimination learning of scratching,but failure to obtain imitation and self-recognition in a long-tailed macaque

A long-tailed macaque was trained to scratch when a model scratched, but failed to generalize scratching when model scratched new target areas. The results confirm that monkeys can control their rates of scratching, but may not be capable of true imitation. The subject also failed on a test of mirror self-recognition. Imitation and self-recognition appear to be related capacities, which may be absent in monkeys.     

Self-agency in rhesus monkeys

Rhesus monkeys (Macaca mulatta) have shown the ability to monitor their own mental states, but fail the mirror self-recognition test. In humans, the sense of self-agency is closely related to self-awareness, and results from monitoring the relationship between intentional, sensorimotor and perceptual information. Humans and rhesus monkeys were trained to move a computer icon with a joystick while a distractor icon partially matched their movements. Both humans and monkeys were able to monitor and identify the icon they were controlling, suggesting they have some understanding of self-agency.     

Display behavior of three troops of Japanese monkeys (Macaca fuscata)

In this paper the display (i.e., “branch-shaking”) behavior of three troops of Japanese monkeys—the confined Oregon troop as reported byModahl andEaton (1977), the semi-free-ranging Arashiyama West troop and the free-ranging Arashiyama B troop—are compared. The comparison reveals several similarities and dissimilarities between the Oregon troop and the two genetically related Arashiyama troops. The similarities include three display postures (shaking, kicking and leaping) and an increased frequency of male but not female displaying during the breeding season. The dissimilarities include the absence of two Oregon display postures (tossing and swinging) and collective displaying among Arashiyama monkeys. The hypothesis ofModahl andEaton (1977) that male displaying influences the females' choice of male mating partners is discussed. The evidence suggests the Oregon monkeys have incorporated male displaying into their socio-sexual behavior to a greater extent than Arashiyama monkeys. However, field observations indicate that males who migrate to the Arashiyama B site during the breeding season can influence female choice by “advertizing” their location with displays.     

Sequential analysis of the social behavior of infants in groups of Japanese monkeys (Macaca fuscata fuscata)

We employed techniques of behavioral entropy to carry out a quantitative analysis of sequences of behavioral patterns evident in the interaction between infants and other members of a group of Japanese monkeys (Macaca fuscata fuscata). The group concerned included examples both of monkeys in captivity and in the wild state. The results were examined as a function of the animal age and environmental differences (cage-field). An example is given to illustrate the use of information theory. Findings partially confirmed that the variability of social behavior decreases as the age of the animals increases.     

Mirrors as environmental enrichment for African green monkeys

Stainless steel circular mirrors were employed in an enrichment plan for 105 singly housed male African green monkeys. We observed 25 randomly selected males to measure mirror use and to assess the mirrors' effectiveness as an enrichment item. We conducted additional mirror-use surveys on all 105 males using fingerprint accumulation as an indicator (rated on a scale of 0 to 4). Use was defined as either being in contact with the mirror (contact use (CU)) or looking directly into the mirror without contact (non-contact use (NC)). Mirror-use data were collected 10 months after the initial introduction of the mirrors and again at 16 months. The two time points were compared by paired t-tests. No significant difference in use was found between the two data collection points. On average, the monkeys used the mirrors 5.2% of the total time intervals recorded (approximately 3 min/hr). Results from the five fingerprint-accumulation surveys showed that 102 of 105 males (97%) had CU with their mirrors over the survey points. Based on the sustained use of the mirrors over a 6-month period, we concluded that the mirrors were an effective enrichment tool that the vast majority of our monkeys routinely used. Habituation did not appear to occur even a year after the mirrors were introduced.     

Disability, compensatory behavior, and innovation in free-ranging adult female Japanese macaques (Macaca fuscata)

Little is known about consequences of disability in nonhuman primates, yet individuals with disabilities can reveal much about behavioral flexibility, innovation, and the capabilities of a species. The Macaca fuscata population surrounding the Awajishima Monkey Center has experienced high rates of congenital limb malformation for at least 40 years, creating a unique opportunity to examine consequences of physical impairment in situ, in a relatively large sample of free-ranging adult monkeys. Here we present behavioral data on 11 disabled adult females and 12 nondisabled controls from 279 hours of randomly ordered 30-minute focal animal follows collected during May-August in 2005, 2006, and 2007. We quantified numerous statistically significant disability-related behavioral differences among females. Disabled females spent less time begging for peanuts from tourists, and employed a behavioral variant of such peanut begging; they had a lower frequency of hand use in grooming and compensated with increased direct use of the mouth or a two-arm pinch technique; and they had a higher frequency of self-scratching, and more use of feet in self-scratching. Self-scratching against substrates was almost exclusively a disability associated behavior. Two females used habitual bipedalism. These differences not withstanding, disabled females behaved similarly to controls in many respects: overall reliance on provisioned and wild foods, time spent feeding, and feeding efficiency did not differ among females, and there was no time difference in behavior performed arboreally or terrestrially. Disabled adult females were able to compensate behaviorally to perform social and life-sustaining activities, modifying existing behaviors to suit their individual physical situations and, occasionally, inventing new ways of doing things.     

Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration

To investigate the problem of inter- and intraspecific differences on the mirror test, we conducted two experiments on cotton-top tamarins. Experiment 1 employed a technique similar to one used recently on chimpanzees, and provided no evidence of mirror-mediated touching of the marked area. In a control condition, involving colored dye applied to one arm, two subjects also failed to show self-directed touching, even though they clearly looked at their newly dyed arm. Under these test conditions, cotton-top tamarins fail to show mirror-guided self-exploration. Experiment 2 examined whether this failure was due to insufficient mirror exposure, as well as other details of the testing conditions. In particular, we replicated the design of a previously successful experiment on mirror-mediated recognition in tamarins [Hauser et al., 1995], providing four new animals with a protracted period (three weeks) of mirror exposure prior to dying their hair. In parallel with results from Experiment 1, we observed no evidence of mirror-mediated behavior (recognition) in Experiment 2.     

Temperament correlates with training success in adult rhesus macaques

In recent years there has been a marked increase in awareness of issues involving the psychological well-being of nonhuman primates (NHPs) used in biomedical research. As a result, many facilities are starting to train primates to voluntarily cooperate with veterinary, husbandry, and research procedures, such as remaining still for blood draws or injections. Such training generally reduces the stress associated with these procedures, resulting in calmer animals and, ultimately, better research models. However, such training requires great investments in time, and there can be vast individual differences in training success. Some animals learn tasks quickly, while others make slower progress in training. In this study, we examined whether temperament, as measured by response to a novel food object, correlated with the amount of time it took to train 20 adult female rhesus macaques to perform a simple task. The monkeys were categorized as "exploratory" (i.e., inspected a novel object placed in the home cage within 10 sec), "moderate" (i.e., inspected the object within 10-180 sec), or "inhibited" (i.e., did not inspect the object within 3 min). We utilized positive reinforcement techniques to train the monkeys to touch a target (PVC pipe shaped like an elbow) hung on their cage. Temperament correlated with training success in this study (Pearson chi2=7.22, df=2, P=0.03). We easily trained over 75% of the animals that inspected the novel food (i.e., exploratory or moderate individuals) to touch the target. However, only 22% of the inhibited monkeys performed the task. By knowing which animals may not respond to conventional training methods, we may be able to develop alternate training techniques to address their specific needs. In addition, these results will allow us to screen monkeys to be assigned to research projects in which they will be trained, with the goal of obtaining the best candidates for those studies.     

Social responding to mirrors in rhesus macaques (Macaca mulatta): Effects of changing mirror location

Two rhesus macaques (Macaca mulatta) with a lifetime of continuous exposure to mirrors showed a dramatic and reliable reinstatement of social behavior directed toward the mirror when it was simply moved to a new location. These data are discussed in the context of repeated failures to find self-recognition in monkeys and several recent claims that a cessation of social behavior directed toward mirrors can be used as evidence for the beginning of self-recognition in nonhuman primates.     

Categorical perception of orientation in monkeys

Structural and functional substrates of orientation processing in monkeys have been clarified. However, orientation perception in monkeys has not been fully studied. In this study, the cognitive mechanism that controls monkeys' perception of orientation was evaluated. After the monkeys were trained to discriminate between a cardinal and an oblique orientation (e.g., 0 degrees and 30 degrees), their perceptual mechanisms underlying orientation discrimination were tested by using six orientations, ranging from 0 degrees to 150 degrees, including ones used in the discrimination training. Generalization tests showed that the monkeys who were trained with cardinal orientations (e.g., 0 degrees) as positive stimuli generalized their responses to the other cardinal orientation (e.g., 90 degrees). Similarly, the monkeys who were trained with oblique orientations (e.g., 30 degrees) as positive stimuli generalized their responses to all other oblique orientations (e.g., 60 degrees, 120 degrees, and 150 degrees). These findings indicated that the monkeys abstracted the quality of the cardinal/oblique category from the physical features of orientation stimuli although they were not trained to do so. Such an abstraction also suggested a discrepancy between a continuously and orderly arranged cortical map and a discontinuously categorized perception of orientation. The present findings provide insight into the learning-correlated plasticity of cortical orientation preference.     

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.     

Species preference by infant macaques with controlled social experience

In Experiment 1, infant Japanese monkeys and rhesus monkeys were artificially reared in pairs with conspecific or heterospecific monkeys. Preferences of these monkeys for a variety of pictures of Japanese monkeys and rhesus monkeys were repeatedly tested during the first 1 or 2 years of life. The duration of lever-pressing responses to see those pictures was a measure of the preference. All monkeys, Japanese or rhesus, preferred pictures of rhesus monkeys to pictures of Japanese monkeys, without regard to their social experiences. Experiment 2, with an adult Japanese monkey as the subject, and Experiment 3, with different pictures as stimuli, suggested that this preference was not a consequence of any bias in the pictures used. In Experiment 4, a Japanese monkey reared by a rhesus foster mother and rhesus monkeys reared by Japanese monkey mothers received the same preference test. The Japanese monkey infant preferred to see pictures of rhesus monkeys. However, rhesus infants did not show clear species preferences. These results suggest that infants of both Japanese and rhesus monkeys have a native tendency to prefer to see physical characteristics of rhesus monkeys over Japanese monkeys.