HP and OG conceived and designed the experiments. HP and AS performed the experiments. HP, AS, and OG analyzed the data, contributed reagents/materials/analysis tools, and wrote the paper.
The authors have declared that no competing interests exist.
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.
A crucial step in the emergence of self-recognition is the understanding that one's own mirror reflection does not represent another individual but oneself. In nonhuman species and in children, the “mark test” has been used as an indicator of self-recognition. In these experiments, subjects are placed in front of a mirror and provided with a mark that cannot be seen directly but is visible in the mirror. Mirror self-recognition has been shown in apes and, recently, in dolphins and elephants. Although experimental evidence in nonmammalian species has been lacking, some birds from the corvid family show skill in tasks that require perspective taking, a likely prerequisite for the occurrence of mirror self-recognition. Using the mark test, we obtained evidence for mirror self-recognition in the European Magpie,
The European magpie, a bird with a large brain and highly developed perspective-taking skills, shows evidence of mirror self-recognition.
Since the pioneering work by Gallup [
Within humans and apes, self-recognition might reflect a homologous trait, whereas findings in other mammals hint at a convergent evolution. A likely reason for such convergent evolution of self-recognition in dolphins and elephants is the convergent evolution of complex social understanding and empathetic behavior [
An investigation of self-recognition in corvids is not only of interest regarding the convergent evolution of social intelligence, it is also valuable for an understanding of the general principles that govern cognitive evolution and their underlying neural mechanisms. Mammals and birds inherited the same brain components from their last common ancestor nearly 300 million years ago and have since then independently developed a relatively large forebrain pallium. However, both classes differ substantially with regard to the internal organization of their pallium, with birds lacking a laminated cortex but having developed an organization of clustered forebrain entities instead [
In the present study, magpies were chosen for several reasons. They are food-storing corvids that compete with conspecifics for individually cached and memorized hoards. They thus live under ecological conditions that favor the evolution of social intelligence [
Mirror behavior in animals goes through several stages. In all species tested so far, inspection of the mirror and social behavior has been observed. In species with mirror self-recognition, some of the individuals also show evidence of inspection of their own body and testing for behavioral contingencies after familiarization with the mirror. For example, they move back and forth in front of the mirror, and this might indicate that they check to which degree the mirror image is coupled to their own movement. Individuals achieving this stage often also pass the mirror and mark test.
In our experiments, we began with open mirror exploration, and then we assessed preference for the mirror and quantified mirror-induced behaviors under highly standardized conditions in a two-compartment cage with one side containing a mirror. Subsequently, we investigated spontaneous self-directed behavior in individuals provided with a mark, and finally, we carried out a series of mark tests and control tests that were designed as to ensure appropriate control and exclude the possibility that findings are due to operant conditioning. Marked individuals (cf.
(A) Attempt to reach the mark with the beak; (B) touching the mark area with the foot; (C) touching the breast region outside the marked area; (D) touching other parts of the body. Behaviors (A) and (B) entered the analysis as mark-directed behavior; behaviors (C) and (D) and similar actions towards other parts of the body were considered self-directed, but not related to the mark.
In baseline trials with a nonreflective plate, there was no remarkable behavior in front of the plate in any of the individuals. With a mirror, the behavior of the magpies clearly differed. Initial exploration of the mirror was characterized by approaches towards the mirror and looks behind the mirror. Also, social behavior occurred, such as aggressive displays towards the mirror and jumping towards the mirror as in a fight. In three individuals, Gerti, Goldie, and Schatzi, social behaviors were transient, i.e., they were reduced already on the second exposure or completely ceased to occur. In the other two birds, Harvey and Lilly, social behaviors, in particular aggressive and submissive displays, continued to be frequent. On several trials, Harvey also picked up little, but conspicuous, objects and posed, accompanied by wing-flipping, in front of the mirror holding the objects in the beak. This courtship-like behavior vanished after a few trials, and was never seen on later tests, which were characterized by aggressive displays. In the open mirror experiment, however, mainly two of the birds (Goldie and Harvey) took part, whereas the other three birds only occasionally visited the location of the mirror. Therefore, we proceeded with a highly standardized protocol for mirror exploration.
In these tests, birds could choose between two identical compartments of a cage, one equipped with a mirror and the other with a nonreflective plate instead of the mirror.
Behavioral Data from Mirror Preference and Standardized Mirror Exploration
In a first exposure to a mirror with a mark, three out of five birds showed at least one instance of spontaneous self-directed behavior (see
Orange bars refer to tests with a colored mark (yellow or red), black bars to tests with a black control mark (sham condition). In Gerti (
Frequencies of Self-Directed Behaviors in the Mark Test
(A) Proportion of mark-directed behavior by Gerti in a test session with change of marks in consecutive 5-min intervals. The color of each bar refers to the color of the mark used and subsequent 5-min periods of the test. Activity towards the mark was high for all colored marks, but low in the control condition (black mark). In all of the color conditions, the bird removed the mark.
(B) Results from the first set of additional controls with a grid in front of the experimental cage instead of a Plexiglas wall. In the colored mark and mirror condition, mark-directed behavior was higher than in the colored mark and no-mirror condition (
Frequencies of Self-Directed Behaviors in the Mark Test
Whereas mark-directed behaviors were virtually absent when the birds were tested without a mirror but with a colored mark, there were a few instances of mark-directed behavior in the mirror condition with a black control mark (
Evidence from the quantitative data is corroborated by the qualitative behavior of the birds. Self-directed activity began after looks into the mirror and visual exploration of the mirror image, and it ceased as soon as the bird had successfully removed the mark (see
Two of the other three birds reacted to the mirror with excited behavior characterized by frequent jumping and running within the cage, and the last bird showed a high number of attacks towards the mirror in one trial (see
Interestingly, the behavior in the mark tests corresponded to interest in the mirror in the standardized mirror exploration test. Those individuals that showed at least one instance of mark-directed behavior were the same that had shown a high interest in the mirror in the preference test, and the individual strongly avoiding the mirror in the choice test (Harvey) showed a high amount of attack-like behavior in the mark test.
One might ask why rather clear evidence was observed in two individuals and weaker evidence in another one, but not in all of the five birds. The proportion of positive findings is, however, well in the range of what has been found in apes. In chimpanzees, the species best studied and showing the clearest evidence of mirror-induced self-directed behavior, a considerable number of individuals typically produce negative findings [
Altogether, results show that magpies are capable of understanding that a mirror image belongs to their own body. We do not claim that the findings demonstrate a level of self-consciousness or self-reflection typical of humans. The findings do however show that magpies respond in the mirror and mark test in a manner so far only clearly found in apes, and, at least suggestively, in dolphins and elephants. This is a remarkable capability that is at least a prerequisite of self-recognition and might play a role in perspective taking. It thus could be essential for the ability of using own experience to predict the behavior of conspecifics [
Brain Weights, Body Weights, as Well as Percent Brain-to-Body Weights of Some of the Different Species That Have Been Tested with Mirrors
We used a small number of tests as it was crucial to ensure that possible self-directed behavior of the birds represented a spontaneous response to seeing the own body in the mirror. Epstein et al. [
Cognitive and neurobiological studies of the last decade have shown that birds and mammals faced a similar selection pressure for complex cognitive abilities, resulting in the evolution of a comparable neural architecture of their forebrain association areas [
Five adult hand-raised magpies served as subjects throughout the study. These birds had been used before in a study on the development of object permanence and in patterned string problems. Investigation of behavior towards a mirror consisted of three steps.
In a 4 × 4-m room, a mirror 55-cm wide and 40-cm high was placed on the ground, leaning against a pole, and slightly tilted. The position of the mirror was in the middle of one of the walls with about 1.5-m distance from the wall, allowing the birds to move around the mirror. The tested subject could move freely in the room. After a baseline trial with the mirror replaced by a grey, nonreflective plate, five test sessions of 30-min duration were given to each of the birds. The behavior of the birds was observed from an adjacent room by means of a video system, and trials were videotaped.
For a quantitative estimation of the interest in the mirror, a cage with two opposite compartments was used. Compartments 60 × 100 × 60 cm (length × height × width) were identical except that there was a mirror at the end of one of the compartments and a grey, nonreflective plate of the same size in the other compartment. Between the compartments, there was a partition with two overlapping walls so that the birds could move freely between compartments but could not see from one compartment into the other. Each of the birds received five consecutive trials of 20 min on separate days. The time the birds spent in the compartment with the mirror was measured, and based of the videotapes bouts of close mirror inspection, looks behind the mirror, bouts of contingent behavior, and social behaviors were counted.
In the mark test, each subject was involved in eight test sessions with the conditions, (1) mirror and colored mark, (2) mirror and black mark, (3) no mirror with colored mark, and (4) no mirror with black mark. One session lasted 20 min. Each condition was replicated once, and two colors, either yellow or red, were used for the colored mark. Thus, our subjects were marked in all conditions to prevent cueing by somesthetic input, but the black mark in condition 2 was practically not visible on the black feathers of the throat. Such sham marking, which also had been used in studies with dolphins and elephants [
Before testing, we protocolled all behaviors observable. Then two observers (others than those assessing the mirror test) independently scored videotapes several times, and a list emerged of 18 behaviors with high interobserver agreement and high reliability over repeated scorings. The list included behaviors not relevant for the question of this study (like moving slowly or fast or jumping in the cage), and for the present study, we focused on a subset of behaviors diagnostic of the animals responding to the mirror. First, social behaviors that could be observed with high reliability were agonistic displays, either submissive or attack-like. During submissive behavior, the bird faces the mirror (or another bird), has its back lowered, its wings slightly spread, and often flips its wings. During aggressive displays, the bird takes an upright position with elongated neck and/or performs attack-like behaviors towards the mirror (c.f. [
Before the first mark test, birds were familiarized with the experimental cage and the mirror for at least 5 d. The experimental cage was 120 × 100 × 60 cm (l × h × w) and had a grid floor. The walls also consisted of a grid except for one long wall, which in most of the tests consisted of Plexiglas in order to provide a good view of the bird. The mirror or the nonreflective plate was always placed on the ground at the same short wall of the cage.
At the beginning of a test, a bird was taken from its home cage and brought to an adjacent room, where the colored mark or the control mark was fixed. The bird was held by one of the experimenters such that the throat region below the beak was exposed. The head of the bird was shielded by the hand of the experimenter holding the bird so that the bird could not see the fixing procedure. The other experimenter then fixed the self-adhesive colored or black mark. Except for the color of the mark, the handling procedure was exactly the same in each of the experimental conditions. Although the dots used for marking were self-adhesive, we prepared them with double-sided adhesive tape in order to ensure good fixation. The weight of a dot was 16 μg and the diameter 8 mm.
After completion of testing of all birds in each of the conditions twice, further tests were applied for the subject Gerti, who showed very clear and consistent self-directed behavior. First of all, a mirror test with four consecutive phases of 5 min was carried out, and in each phase, a new mark was fixed (yellow, blue, black, or red). Secondly, additional tests comparing the behavior in the colored mark and mirror condition with that in the colored mark and no-mirror condition were carried out with a normal cage grid instead of a Plexiglas wall in front of the cage. In experiments with dolphins [
While the birds were being set into or removed from the experimental cage, room lights were switched off. A test began by turning the lights on. Experiments were monitored via a video system from an adjacent room, and all tests were videotaped. From videotapes, the frequency of behaviors directed towards the own body were scored. Actions towards the marked region with the beak or the foot entered the analysis as mark-directed behavior (see
Nine video clips that show relevant behavioral sequences for the subjects Gerti, Goldie, Harvey, and Schatzi.
The bird is close to the mirror, behaves in a rather quiet way, and explores its mirror image. This behavior contrasts sharply with the agitated and sometimes aggressive behavior as observed in the subjects Harvey and Lilly (see
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The bird had a strong preference for the compartment with the mirror and explored the situation intensively. Note the repeated sequences of looks into the mirror and behind the mirror.
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Gerti is testing for contingencies between her own behavior and the mirror image by moving back and forth and left and right in front of the mirror. Note the behavior after 20 s when Gerti very slowly bends to the left and inspects her mirror image with the mark. We never observed similar behavior in any social interaction between two magpies.
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Goldie explores his mirror image while moving back and forth and turning his head in front of the mirror.
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Gerti tries to reach the mark with the beak, which is not possible. In the second of the two scenes, she finally takes her right foot and successfully removes the mark.
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Schatzi attempts to reach the mark with the right foot.
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Three examples of mark-directed behavior with the foot by Gerti. The three examples show how the birds used their feet for mark-directed behavior. They also show that this behavior, as with mark-directed behavior with the beak, is clearly distinguishable from actions towards other parts of the body.
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The example shows how Gerti tried to support mark removal with the beak by means of bill swipes. Note that after having removed the mark, Gerti turns to the mirror and inspects her mirror image before beginning comfort behavior.
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Four instances of social, in particular, aggressive behavior in the subject Harvey. In the first two scenes, the behavior shows a transition between submissive and aggressive behavior; the last two scenes represent outright attack-like behavior.
In some of the scenes filmed at an early stage of the experiments, Gerti was in a phase of molting. Later scenes show the same subject with full plumage after molting had ceased. Note that birds with lateral eyes fixate objects by viewing laterally with either the right or left eye.
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