Mirrors as enrichment for captive chimpanzees (Pan troglodytes).

At many facilities, limitations of the physical environment have reduced the opportunity for captive chimpanzees to live in large, naturalistic social groups. Convex mirrors used to increase visual access of neighboring groups may improve the social environment. This was tested in a study of 28 chimpanzees (Pan troglodytes) group-housed in conventional indoor/outdoor runs. A total of 47.8 hours of behavioral observations were conducted and comparisons made across three conditions: no mirror present, a mirror present with visual access to neighboring conspecifics, or a mirror present with visual access to the neighbors' empty run. When the mirror gave subjects visual access to neighboring animals, facial expressions, sexual, and agonistic behaviors increased, whereas affiliative behavior decreased compared with when no mirror was present. When the mirror gave subjects visual access to a neighbors' empty run, facial expressions and sexual behavior increased compared with when no mirror was present. When the mirror gave subjects visual access to a neighbor's empty run, agonism decreased compared with when a mirror gave subjects visual access to neighboring animals. When subjects had visual access to neighbors, they used the mirror 30% of the total data points; while they had visual access to the neighbors' empty run, they looked during 24% of the total data points. Juveniles' use of the mirror increased over time while adults' use remained stable. Adult males used the mirror less than did the other subjects. These findings indicate that a mirror allowing visual access to neighboring conspecifics has potential as an enrichment device that affects social behavior.     

Responses of capuchin monkeys (Cebus apella) to different conditions of mirror-image stimulation

Group-living brown capuchins were given mirror-image stimulation as follows: (1) mirror 1 m away; (2) mirror attached to the cage-mesh; (3) angled mirrors creating a deflected image; (4) small mirror in the cage; and (5) small, transportable mirrors. The subjects were initially interested in the mirrors in each condition, but they generally habituated to them over the course of repeated presentations. Control (non-reflective) objects were attended to less than mirrors. Facial expressions occurred mostly in Condition 2, lateral and vertical head movements in Condition 3, reaching behind the mirror in Condition 2, looking obliquely into the mirror in Conditions 4 and 5. Despite these diverse conditions of exposure to mirrors, lasting for a total of over three months, no behaviours suggesting self-recognition were seen in the monkeys.     

Long-term use of televisions,balls, and mirrors as enrichment for paired and singly caged chimpanzees

The evaluation of environmental enrichment techniques for nonhuman primates over long periods of time has had mixed results. Some studies report rapid habituation to new enrichment items, while others note continued use. We have investigated the use of three different enrichments that had been available to paired and singly caged chimpanzees for several years. Twenty subjects were observed during 200 hr of scan sampling while singly caged and while pair housed. Each subject had a variety of enrichments available and their use of a television, ball, and mirror were recorded. The chimpanzees had previous exposure to all of the items: televisions had been available for a mean of 22.75 months, balls had been available for 55.9 months, and mirrors had been available for 25.9 months. The results indicated that the chimpanzees continued to use the enrichments for small amounts of time (0.27%–1.53% of the observations) even after such prolonged exposure. Television and ball use were significantly higher than mirror use. Housing condition was not a significant factor in the analyses, contrary to expectations. We concluded that several simple enrichment items may be effective in offering variety and choices to the nonhuman primate and can be one element in a comprehensive environmental enhancement plan. © 1996 Wiley-Liss, Inc.     

Mirror reactions in a zoo colony of Cebus monkeys

The extensive research investigating the reactions of a number of species of nonhuman primates to their mirror images has revealed that monkeys have never been observed to react with self-directed behaviors, as have some species of higher apes. The intermittent exposure of captive Cebus monkeys to a mirror over a 5-week period produced species-specific social reactions to the mirror, supporting the suggestion that at least in some instances the monkeys were viewing their mirror image as a conspecific. The variability in the duration and expression of mirror-directed behaviors observed in the study appeared to be related to the age and past experience of the monkeys. The duration of mirror viewing of subadults was over twice that of the adults, while the young, hand-reared animals exhibited more manipulative and fewer social behaviors than did the young animals raised in the zoo. The average viewing time of the zoo colony decreased substantially over the course of the study but the monkeys were still spending an appreciable time at the mirror after 5 weeks.     

Approach of females to magnified reflections indicates that claw size of waving fiddler crabs correlates with signaling effectiveness

Male sand fiddler crabs, Uca pugilator, wave a claw to attract females to a breeding burrow. The effect of claw size on the likelihood of attracting mate-seeking females is little studied although in some other species females preferentially approach larger males. We used paired mirrors to reflect different sized images of the same male in a South Carolina (USA) back-beach habitat. Use of mirrors controlled for waving rate (but not velocity), waving motion, claw color, and claw shape. Female choice was attributed to instances in which a female contacted one of two mirrors. Paired mirrors were inclined toward one another in an arena defined by blinds and containing a single male. Two reflections of the male were visible to females moving approximately 50 cm toward the mirrors. The male was behind a small internal blind and not directly visible. In one-half of the trials, a non-magnifying mirror was placed at the bottom of mirrors so that only the elevated claw was magnified. Thus, body and burrow size and apparent distance were controlled. Receptive females preferred the larger reflection whether or not the body of the male was magnified, suggesting the importance of claw size. Non-receptive females did not exercise a choice. Control arenas, without a male, rarely attracted females. The results suggest that females choose on the basis of claw size. Selection on females may favor response to larger-clawed males because use of the claw in contests between males over burrows maintains the honesty of claw size as a signal of burrow quality.     

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.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

Responses of female rhesus macaques to an environmental enrichment apparatus

Environmental enrichment devices are a potential way to enhance psychological well-being in laboratory animals. The effects of such devices need to be systematically evaluated before they are recommended for widespread use. The purpose of this research was to monitor the behavioural and physiological responses of adult female rhesus macaques to a simple enrichment device. The apparatus consisted of a box attached to the monkey's home cage that contained a radio and a food dispenser, which could be controlled by the monkeys via contact detectors. Radio and food dispenser use were automatically recorded. Whole blood serotonin (WBS), plasma cortisol and abnormal behaviour were measured in 5 monkeys before, during and after a 20-week period in which the monkey's cages were equipped with the device. All monkeys used the device (3 of the 5 subjects earned an average of more than 200 food pellets per day). Mean plasma cortisol and whole blood serotonin did not differ across sampling times, suggesting that the apparatus had no effect on basal stress levels. There was an inverse relationship between apparatus use and cortisol levels in 76% of the samples, but only 3 of 17 coefficients were significant. There was a significant but small negative correlation between apparatus use and self-abusive behaviour. This enrichment device was readily used by adult rhesus monkeys and could be adapted for use in a wide variety of laboratory settings.     

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.     

Rhesus Monkeys (Macaca mulatta) Do Recognize Themselves in the Mirror: Implications for the Evolution of Self-Recognition

Self-recognition in front of a mirror is used as an indicator of self-awareness. Along with humans, some chimpanzees and orangutans have been shown to be self-aware using the mark test. Monkeys are conspicuously absent from this list because they fail the mark test and show persistent signs of social responses to mirrors despite prolonged exposure, which has been interpreted as evidence of a cognitive divide between hominoids and other species. In stark contrast with those reports, the rhesus monkeys in this study, who had been prepared for electrophysiological recordings with a head implant, showed consistent self-directed behaviors in front of the mirror and showed social responses that subsided quickly during the first experimental session. The self-directed behaviors, which were performed in front of the mirror and did not take place in its absence, included extensive observation of the implant and genital areas that cannot be observed directly without a mirror. We hypothesize that the head implant, a most salient mark, prompted the monkeys to overcome gaze aversion inhibition or lack of interest in order to look and examine themselves in front of the mirror. The results of this study demonstrate that rhesus monkeys do recognize themselves in the mirror and, therefore, have some form of self-awareness. Accordingly, instead of a cognitive divide, they support the notion of an evolutionary continuity of mental functions.     

Use of a mirror to direct their responses in Japanese monkeys (Macaca fuscata fuscata)

Two male Japanese monkeys used a mirror to inspect an object attached to their bodies but not directly visible. These monkeys had been trained previously to use a mirror to guide their hand to a target. In Experiment 1 their behavior in the presence of a mirror was observed. In Experiment 2 the monkeys used the mirror to locate a picture projected on a screen to the left or right rear side of the cage. In Experiment 3 the monkeys used a mirror to observe and finally grasp an object attached behind their heads. Two monkeys who were not trained to use a mirror to obtain an otherwise hidden object did not show such behavior.     

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.     

What mirror self-recognition in nonhumans can tell us about aspects of self

Research on mirror self-recognition where animals are observed for mirror-guided self-directed behaviour has predominated the empirical approach to self-awareness in nonhuman primates. The ability to direct behaviour to previously unseen parts of the body such as the inside of the mouth, or grooming the eye by aid of mirrors has been interpreted as recognition of self and evidence of a self-concept. Three decades of research has revealed that contrary to monkeys, most great apes (humans, common chimpanzees, pygmy chimpanzees and orangutans but not the gorilla) have convincingly displayed the capacity to recognize self by mirrors. The putative discontinuity in phylogeny of the ability suggests the existence of a so-called cognitive gap between great apes and the rest of the animal kingdom. However, methodological and theoretical inconsistencies regarding the empirical approach prevail. For instance, the observation of self-directed behaviour might not be as straightforward as it seems. In addition, the interpretation of mirror self-recognition as an index of self-awareness is challenged by alternative explanations, raising doubt about some assumptions behind mirror self-recognition. To evaluate the significance of the test in discussions of the concept of self this paper presents and analyses some major arguments raised on the mirror task.     

Changes in gonadotrope responsivity to gonadotropin releasing hormone during development of the rhesus monkey

To assess the changing responsiveness of pituitary gonadotropes to gonadotropin releasing hormone (GnRH) during development, 5 male and 5 female rhesus monkeys were studied. Three monkeys of each sex were tested periodically with a subcutaneous injection of 500 micrograms of GnRH dissolved in 50% polyvinylpyrrolidone (PVP) beginning at 2 to 4 weeks of age and continuing into young adulthood. The remaining 4 monkeys received injections of the vehicle (PVP) alone and served as controls. Serum concentrations of bioactive luteinizing hormone (LH) were determined by an interstitial cell testosterone bioassay, and follicle-stimulating hormone (FSH) levels were measured by radioimmunoassay. Baseline FSH levels in the 5 female neonatal monkeys were higher than those of the 5 male neonatal monkeys during the first 2 months of life. In both sexes, FSH concentrations decreased with age, and FSH was barely detectable by 6 months. Baseline LH values in the 5 female monkeys declined during the first 6 months of the study and were undetectable (less than 0.5 micrograms/ml) at 6 months of age. Baseline LH levels in 4 of the 5 neonatal males also declined to undetectable concentrations by 6 months of age. During the first 3 months of life, there was a striking increase in the serum concentrations of both LH and FSH following GnRH. Although the LH responses to GnRH (delta LH) were similar in males and females of comparable ages, the FSH responses (delta FSH) were considerably greater in the female monkeys. In the males, the delta LH exceeded the delta FSH, whereas in the females, the delta FSH were greater than the delta FSH. In both sexes, the delta LH and delta FSH generally were greatest in the youngest monkeys and decreased gradually with increasing age. By 6 months, the gonadotropin responses to GnRH either were undetectable (males) or very small (females). After 6 months there was no longer an increase in serum gonadotropins after GnRH in either sex until 1.5-4 years (females) or 3 years (males) of age. The delta LH in response to GnRH in the male monkeys 3-5 years of age were comparable to the responses during the first month after birth. Serum concentrations of FSH in the adult males, however, did not increase after GnRH. In the female monkeys, serum levels of LH and FSH increased after GnRH at 1.5 years (1 monkey) and 4 years (2 monkeys) of age. The delta LH were similar to those of the 1- to 2-month-old female monkeys. The delta FSH, however, were variable and were approximately 20% of the neonatal response. In these young adult female monkeys the delta LH exceeded the delta FSH.(ABSTRACT TRUNCATED AT 400 WORDS)     

Distribution and abundance of patas monkeys (Erythrocebus patas) in Laikipia, Kenya, 1979-2004

Patas monkeys may be especially vulnerable to local extinction because they live in relatively small, female-philopatric groups at low densities and are strongly polygynous. We assessed a patas monkey population in Kenya's 9,700 km(2) Laikipia District over 25 years, using data collected in 1979-1981 and 1992-2004. The data were based on intensive observations of three study groups, "on the ground" counts, and surveys of Laikipia residents. In 1979-1981, a minimum of 415 patas monkeys lived in 14-15 groups. By 2000, the best estimate suggested 310-445 patas monkeys living in 13-17 groups over a greater surveyed area, suggesting that patas monkeys in Laikipia may have undergone a slight decline in numbers over time. Their distribution, however, was similar over time. The relative stability of this population has likely been the result of beneficial co-existence with large-scale cattle ranching. Outside Laikipia, substantial habitat alteration from rising human populations has coincided with the near disappearance of patas monkeys where they were previously more numerous. The small population in Laikipia, probably the largest remaining in Kenya, may therefore be critical to the continued existence of patas monkeys in that country and may be dependent on maintenance of large-scale ranches. Such land use provides patas monkeys with water and broad expanses of Acacia drepanolobium woodlands, the habitat to which patas are restricted in Laikipia.     

Monkeys with mirrors: Some questions for primate psychology

Monkeys do not appear to recognize themselves in mirrors but display social responses to the reflection. This article comprehensively reviews the literature concerning monkeys’ reactions to mirrors, describing the interest shown in reflections, the reinforcing effects of mirror-image stimulation, the social responses of the monkeys, their interpretation of objects reflected in a mirror, and their performance in tests of self-recognition. In all cases limitations of the methods employed restrict conclusions about the monkeys’ behavior. Detailed behavioral observations coupled with comparisons of the psychological properties of mirrors with those of other stimuli promise to reveal more useful information about cognitive mechanisms and abilities of monkeys and other primates.     

Pickle barrels as enrichment objects for rhesus macaques.

Two breeding groups of rhesus monkeys (Macaca mulatta) housed in outdoor enclosures on Key Lois island were observed for 84 hours. Instantaneous scan sampling of a focal animal was used to gather data to test hypotheses concerning frequencies of agonistic and affiliative behaviors as well as differential use of pickle barrels as enrichment objects. Type of barrel used, behavior, and age/sex class of the animal were noted. Barrels were arranged three ways: unattached, on a swivel, and stationary. The behaviors of animals in an enriched environment were compared with control condition animals, which did not have pickle barrels. Animals in an enriched environment accounted for 60.8% (n = 56) of total affiliative contact, 62.2% (n = 399) of total social grooming, and 26% (n = 5) of total agonistic noncontact. A total of 134 scans of barrel use were observed. Analyses of the data showed that swivel and stationary barrels were used the most (55% of all scans of barrel use). Yearlings, juvenile females, and old males used barrels most often (82.8% of all scans of barrel use), although they constituted only 39% of the enriched environment population. In this study, pickle barrels provided enrichment for young and old animals of both sexes.     

The feeding ecology and activity budget of proboscis monkeys

A group of proboscis monkeys (Nasalis larvatus) consisting of an alpha‐male, six adult females, and several immatures was observed from May 2005–2006. We collected over 1,968 hr of focal data on the adult male and 1,539 hr of focal data on the six females in a forest along the Menanggul River, Sabah, Malaysia. Availability and seasonal changes in plant species consumed by the focal monkeys were determined by vegetation surveys carried out across an area of 2.15 ha along 200–500 m trails in riverine forest. A total of 188 plant species were consumed by the focal monkeys. The activity budget of members of our study group was 76.5% resting, 19.5% feeding, and 3.5% moving. Young leaves (65.9%) and fruits (25.9%) accounted for the majority of feeding time. Over 90% of fruit feeding involved the consumption of unripe fruits and in the majority of case both the fruit flesh and seeds were eaten. Although fruit eating was rare in some months, during other times of the year time fruit feeding exceeded the time devoted to young leaves. We found that monthly fruit availability was positively related to monthly fruit eating and feeding activity, and seasonal fluctuations in dietary diversity were significantly affected by fruit eating. These results suggest that fruit availability and fruit‐eating behaviors are key factors that influence the activity budget of proboscis monkeys. Earlier assumptions that colobine monkeys are obligate folivores do not apply well to proboscis monkeys and certain other colobines. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of Asian colobines. Am. J. Primatol. 71:478–492, 2009. © 2009 Wiley‐Liss, Inc.     

Cage toys reduce abnormal behavior in individually housed pigtail macaques

As part of a behavioral intervention program that identifies and treats individual nonhuman primates exhibiting abnormal behavior, five individually housed pigtail macaques (Macaca nemestrina) were provided with multiple cage toys in an effort to reduce high levels of abnormal behavior. Ten 30-min observations of each subject were conducted during the baseline condition and again after novel toys were presented, both loose inside the cage and attached to the outside of the cage. The new toys were used during 27% of the observation time. Kong Toys were used most consistently by the macaques during the 5-week observation period. Significant decreases in abnormal behavior and cage-directed behavior, as well as significantly increased enrichment use, were evident after the toys were added. Several of the toys were destroyed quickly, and individual differences were evident in the levels of enrichment use and abnormal behavior. Providing multiple manipulable toys as enrichment for pigtail macaques was effective in reducing abnormal behavior and was an important part of an environmental enrichment program for monkeys who could not be housed socially.