Mirror-mediated responses of California scrub jays (Aphelocoma californica) during a caching task and the mark test

Mirror self-recognition, as an index of self-awareness, has been proposed as a precursor for more complex social cognitive abilities, such as prosocial reasoning and cooperative decision-making. Indeed, evidence for mirror self-recognition has been shown for animals possessing complex social cognitive abilities such as great apes, dolphins, elephants and corvids. California scrub jays (Aphelocoma californica) have provided strong evidence that non-human animals are capable of mental state attribution. For instance, scrub jays are reported to use their experience stealing the food of others to infer that other birds may similarly intend to steal from them. If a concept of “self” is required for such complex social cognitive abilities, then scrub jays might be expected to show mirror self-recognition. Thus, we examined whether California scrub jays are capable of mirror self-recognition using two experimental contexts: a caching task and the mark test. During the caching task, we compared the extent to which scrub jays protected their food after caching alone, in the presence of a conspecific and in the presence of a mirror. The birds did not engage in more cache protection behaviours with a mirror present than when caching alone, suggesting scrub jays may have recognized their reflection and so did not expect cache theft. Alternative explanations for this behaviour are also discussed. During the mark test, the scrub jays were surreptitiously marked with a red or plumage-coloured control sticker. The scrub jays showed no evidence of mirror self-recognition during the mark test, as the birds did not preferentially attempt to remove the red mark in the presence of a mirror. Together, the results provide mixed evidence of the mirror self-recognition abilities of California scrub jays. We highlight the need to develop alternative approaches for evaluating mirror self-recognition in non-human animals to better understand its relationship with complex social cognition.     

Mirror responses in a group of Miopithecus talapoin

Studies of non-human primate self-recognition in mirrors demonstrate variation both within and between species. This study applied a rigorous methodology that took into account habituation of subjects to the mirror as an object and to the experimental situation. The species observed in our study was Miopithecus talapoin, which has been little studied in the wild or in captivity. Although this species shows several interesting characteristics, including complex social organisation and a high encephalization index, the talapoin monkeys in the study did not pass the mark test; however, they showed a prerequisite for self-recognition, namely comparing their body parts to the image of these in the mirror.     

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.     

Mirror-Mark Tests Performed on Jackdaws Reveal Potential Methodological Problems in the Use of Stickers in Avian Mark-Test Studies

Some animals are capable of recognizing themselves in a mirror, which is considered to be demonstrated by passing the mark test. Mirror self-recognition capacity has been found in just a few mammals having very large brains and only in one bird, the magpie (Pica pica). The results obtained in magpies have enormous biological and cognitive implications because the fact that magpies were able to pass the mark test meant that this species is at the same cognitive level with great apes, that mirror self-recognition has evolved independently in the magpie and great apes (which diverged 300 million years ago), and that the neocortex (which is not present in the bird''s brains) is not a prerequisite for mirror self-recognition as previously believed. Here, we have replicated the experimental design used on magpies to determine whether jackdaws (Corvus monedula) are also capable of mirror self-recognition by passing the mark test. We found that our nine jackdaws showed a very high interest towards the mirror and exhibited self-contingent behavior as soon as mirrors were introduced. However, jackdaws were not able to pass the mark test: both sticker-directed actions and sticker removal were performed with a similar frequency in both the cardboard (control) and the mirror conditions. We conclude that our jackdaws'' behaviour raises non-trivial questions about the methodology used in the avian mark test. Our study suggests that the use of self-adhesive stickers on sensitive throat feathers may open the way to artefactual results because birds might perceive the stickers tactilely.     

Not all chimpanzees (Pan troglodytes) show self-recognition

When a chimpanzee is presented with a mirror it initially responds with social behavior directed toward the reflection. After several hours of exposure to the mirror the social behavior decreases and the mirror is used to guide self-directed responses to previously unobservable parts of the body such as the face. When a distinctively colored mark is unobtrousively applied to the chimpanzee's face and the chimpanzee touches the mark while observing itself in the mirror, this behavior is said to indicate self-recognition. Such self-recognition has been considered to be a robust phenomenon in chimpanzees, with self-directed and mark-directed behaviors both appearing in all socially-housed adult chimpanzees tested. In our study 11 chimpanzees were given mirror exposure and tested with the mark test. Only one of the 11 chimpanzees touched the mark during test, although several showed self-directed behavior using the mirror to guide their movements. Such experimental factors as mirror size, position, or temporal spacing of the mirror exposure, and such subject variables as age, sex, previous social experience, and subspecies were insufficient to explain the difference between the present and previous findings. We suggest that there are individual differences in mirror recognition behavior in chimpanzees, and that further consideration of the factors contributing to this phenomenon, including the development of additional tests for self-recognition, is needed.     

Failure to demonstrate self-recognition in gorillas

Two zoo-reared gorillas were each given nearly 400 h of mirror exposure. Extensive mirror gazing and social behaviors were exhibited, the frequency of which decreased gradually over the study period. Neither animal demonstrated the transition from other-directed to self-directed behavior characteristic of both chimpanzees and orangutans, and no evidence of self-recognition was found using the Gallup marking paradigm. These negative findings, after extensive mirror exposure, suggest that the gorilla may be the only great ape which lacks the conceptual ability necessary for self-recognition.     

Contingency checking and self-directed behaviors in giant manta rays: Do elasmobranchs have self-awareness?

Elaborate cognitive skills arose independently in different taxonomic groups. Self-recognition is conventionally identified by the understanding that one’s own mirror reflection does not represent another individual but oneself, which has never been proven in any elasmobranch species to date. Manta rays have a high encephalization quotient, similar to those species that have passed the mirror self-recognition test, and possess the largest brain of all fish species. In this study, mirror exposure experiments were conducted on two captive giant manta rays to document their response to their mirror image. The manta rays did not show signs of social interaction with their mirror image. However, frequent unusual and repetitive movements in front of the mirror suggested contingency checking; in addition, unusual self-directed behaviors could be identified when the manta rays were exposed to the mirror. The present study shows evidence for behavioral responses to a mirror that are prerequisite of self-awareness and which has been used to confirm self-recognition in apes.     

Further evidence for the capacity of mirror self-recognition in cleaner fish and the significance of ecologically relevant marks

An animal that tries to remove a mark from its body that is only visible when looking into a mirror displays the capacity for mirror self-recognition (MSR), which has been interpreted as evidence for self-awareness. Conservative interpretations of existing data conclude that convincing evidence for MSR is currently restricted to great apes. Here, we address proposed shortcomings of a previous study on MSR in the cleaner wrasse Labroides dimidiatus, by varying preexposure to mirrors and by marking individuals with different colors. We found that (1) 14/14 new individuals scraped their throat when a brown mark had been provisioned, but only in the presence of a mirror; (2) blue and green color marks did not elicit scraping; (3) intentionally injecting the mark deeper beneath the skin reliably elicited spontaneous scraping in the absence of a mirror; (4) mirror-naive individuals injected with a brown mark scraped their throat with lower probability and/or lower frequency compared to mirror-experienced individuals; (5) in contrast to the mirror images, seeing another fish with the same marking did not induce throat scraping; and (6) moving the mirror to another location did not elicit renewed aggression in mirror-experienced individuals. Taken together, these results increase our confidence that cleaner fish indeed pass the mark test, although only if it is presented in ecologically relevant contexts. Therefore, we reiterate the conclusion of the previous study that either self-awareness in animals or the validity of the mirror test needs to be revised.

When animal tries to remove a mark from its body that is only visible when looking into a mirror (the "mark test"), it displays the capacity for mirror self-recognition, often interpreted as evidence for self-awareness. This follow-up to a previous PLOS Biology study increases confidence that cleaner fish indeed pass the mark test, but only if it is presented in ecologically relevant contexts.     

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.     

A new mark test for mirror self-recognition in non-human primates

For 30 years Gallups (Science 167:86–87, 1970) mark test, which consists of confronting a mirror-experienced test animal with its own previously altered mirror image, usually a color mark on forehead, eyebrow or ear, has delivered valuable results about the distribution of visual self-recognition in non-human primates. Chimpanzees, bonobos, orangutans and, less frequently, gorillas can learn to correctly understand the reflection of their body in a mirror. However, the standard version of the mark test is good only for positively proving the existence of self-recognition. Conclusive statements about the lack of self-recognition are more difficult because of the methodological constraints of the test. This situation has led to a persistent controversy about the power of Gallups original technique. We devised a new variant of the test which permits more unequivocal decisions about both the presence and absence of self-recognition. This new procedure was tested with marmoset monkeys (Callithrix jacchus), following extensive training with mirror-related tasks to facilitate performance in the standard mark test. The results show that a slightly altered mark test with a new marking substance (chocolate cream) can help to reliably discriminate between true negative results, indicating a real lack of ability to recognize oneself in a mirror, from false negative results that are due to methodological particularities of the standard test. Finally, an evolutionary hypothesis is put forward as to why many primates can use a mirror instrumentally – i.e. know how to use it for grasping at hidden objects – while failing in the decisive mark test.To see a video sequence of the instrumental use of mirror by Callithrix jacchus as described in this study, please go to     

A developmental approach to the origins of self-recognition in great apes

In this paper I present an hypothesis to explain the presence of mirror self-recognition (MSR) in great apes and human infants, and the absence of MSR in monkeys. This hypothesis is based on the following elements: 1) review of Gallupian studies of MSR in monkeys and apes; 2) review of Lewis & Brooks-Gunn's study for self-recognition in human infants; 3) application of the human model to comparative data on MSR in nonhuman primates; 4) discussion of cognitive correlates of MSR in human infants; 5) analysis of the cognitive correlates of MSR absence in monkeys, and MSR presence in apes; 6) comparative analysis of the modalities of occurrence of imitation and understanding of causality in monkeys and apes; and 7) a cladistic reconstruction of the evolution of MSR.     

Mirror image processing in three marine mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus)

Dolphins (Tursiops truncatus) and their relatives might be expected to show mirror-induced contingency checking, a prerequisite to self-recognition, because of their high brain development, their complex social life and their demonstrated abilities in bodily imitation. A study of killer whales'(Orcinus orca) behaviour in front of a mirror is presented, including a mark test. Shorter investigations of mirror behaviour are also described in false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus). Contingency checking was present in killer whales and possibly also in false killer whales, but no clear contingency checking was observed in sea lions. The mark test on killer whales suggested that the marked animal anticipated that its image would look different. This study shows that killer whales and false killer whales, like bottlenose dolphins, appear to possess the cognitive abilities required for self-recognition.     

Mirror responses in a Japanese macaque troop (Arashiyama West)

Behavior toward two mirrors in the field was observed in the Arashiyama West troop ofMacaca fuscata. Counts of visits to the mirrors, plus scan and focal animal sampling were used. Some animals were marked with fluorescent paint to test informally for self-recognition. A relatively high mean frequency of visits to the reflecting side of both mirrors by all age classes, ranks, and sexes was recorded. There was no age difference in frequency of mirror visits per sample but adults spent more time per visit than subadults who in turn spent more time than juveniles. There was no indication of self-recognition by paint-marked animals. Mirrors appeared to be used to monitor the reflected scene and to look at the self-image. Social behavior in the mirror zone that was not directed toward the mirror was common to all age classes. Species-typical behavior directed toward the mirror was seen in younger animals but very seldom in adults. No threat displays by any animal were observed. We suggest that for adults the mirror image was not seen simply as another monkey.     

Do rhesus monkeys recognize themselves in mirrors?

Self-recognition continues to attract attention because of the evidence of a striking difference between the great apes and humans, on the one hand, and all other primates; the former are capable of self recognition,whereas no compelling evidence exists for prosimians, monkeys, or lesser apes. This is inspite of numerous attempts to facilitate mirror self-recognition in other primates. Although all previous attempts to find self-recognition in rhesus macaques have failed, a recent article [Rajala et al., PLoS One9:e12865, 2010] claimed the opposite—that adult male rhesus monkeys did recognize their own image in a mirror. We critically examine this claim, and conclude that the article fails to provide acceptable evidence for self-recognition in rhesus monkeys.     

Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition

Comparative studies suggest that at least some bird species have evolved mental skills similar to those found in humans and apes. This is indicated by feats such as tool use, episodic-like memory, and the ability to use one's own experience in predicting the behavior of conspecifics. It is, however, not yet clear whether these skills are accompanied by an understanding of the self. In apes, self-directed behavior in response to a mirror has been taken as evidence of self-recognition. We investigated mirror-induced behavior in the magpie, a songbird species from the crow family. As in apes, some individuals behaved in front of the mirror as if they were testing behavioral contingencies. When provided with a mark, magpies showed spontaneous mark-directed behavior. Our findings provide the first evidence of mirror self-recognition in a non-mammalian species. They suggest that essential components of human self-recognition have evolved independently in different vertebrate classes with a separate evolutionary history.     

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.     

Why do chimpanzees have diverse behavioral repertoires yet lack more complex cultures? Invention and social information use in a cumulative task

Humans are distinctive in their dependence upon products of culture for survival, products that have evolved cumulatively over generations such that many cannot now be created by a single individual. Why the cultural capacity of humans appears unrivalled in the animal kingdom is a topic of ongoing debate. Here we explore whether innovation and/or social learning propensities may constrain the ability of one of our closest living relatives, chimpanzees (Pan troglodytes), to master an extractive foraging and tool-use task designed to afford opportunities for cumulative culture to develop. We further explore the potential demographic characteristics associated with novel task solutions. Chimpanzees (N = 53) were inventive, flexibly exploring the novel task, albeit complex inventions were rare and shaped by prior individual experience with similar tool-use tasks. However, they displayed no evidence of cumulative cultural learning. Communities displayed richer behavioral repertoires and had greater task success than chimpanzees tested in an asocial control condition, but their solution complexity did not surpass what individuals invented. The lack of social transmission of complex and beneficial solutions in contexts like those we studied provides one explanation for the limited cumulative culture observed in this species.     

Monkeys,apes, mirrors and minds: The evolution of self-awareness in primates

Almost two decades of research on the self-recognition capacity of non-human primates has produced evidence of intriguing phylogenetic differences. Not a single species of monkey has demonstrated the ability to recognize its own reflection in a mirror, despite some claims to the contrary. To date, only humans, orangutans and chimpanzees have passed objective tests of mirror-recognition. This paper reviews the methodology and evidence for self-recognition in primates along with the assumption that this ability is an indicator of self-awareness. The failure of the gorilla to master the task is discussed in some detail, along with an evaluation of anecdotal evidence of self-recognition by at least one gorilla. Also, the evolutionary backdrop of the primates is considered with reference to this unique behavior. Evidence supporting alternate, non-cognitive interpretations of self-recognition is assessed.     

Ontogeny of mirror behavior in two species of great apes

Mirror image reactions of two infant apes, a female chimpanzee (Pan troglodytes) and a male orangutan (Pongo pygmaeus), born at the Zoo de Vincennes and the Jardin des Plantes of Paris, France, respectively, were studied and compared with those of children. Self-recognition was also tested following 46.5 hours of mirror exposure by application of red marks on parts of the body invisible to the animal without the aid of the mirror. Results indicated that the behavior of the two young apes followed a developmental trend similar to that of human babies. At the end of the study, the female chimpanzee (11 months of age) expressed social behavior, searched for the image behind the mirror, and showed interest in imaged movement. The orangutan (2 years and 5 months old) had begun to test movement synchronism and to display self-directed behaviors. The tests of self-recognition yielded negative results in both animals.     

Mirror self-recognition and symbol-mindedness

The view that mirror self-recognition (MSR) is a definitive demonstration of self-awareness is far from universally accepted, and those who do support the view need a more robust argument than the mere assumption that self-recognition implies a self-concept (e.g. Gallup in Socioecology and Psychology of Primates, Mouton, Hague, 1975; Gallup and Suarez in Psychological Perspectives on the Self, vol 3, Erlbaum, Hillsdale, 1986). In this paper I offer a new argument in favour of the view that MSR shows self-awareness by examining the nature of the mirror image itself. I argue, using the results of ‘symbol-mindedness’ experiments by Deloache (Trends Cogn Sci 8(2):66–70, 2004), that where self-recognition exists, the mirror image must be functioning as a symbol from the perspective of the subject and the subject must therefore be ‘symbol-minded’ and hence concept possessing. Further to this, according to the Concept Possession Hypothesis of Self-Consciousness (Savanah in Conscious Cogn 2011), concept possession alone is sufficient to demonstrate the existence of self-awareness. Thus MSR as a demonstration of symbol-mindedness implies the existence of self-awareness. I begin by defending the ‘mark test’ protocol as a robust methodology for determining self-recognition. Then follows a critical examination of the extreme views both for and against the interpretation of MSR as an indication of self-awareness: although the non-mentalistic interpretation of MSR is unconvincing, the argument presented by Gallup is also inadequate. I then present the symbol-mindedness argument to fill in the gaps in the Gallup approach.