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. Table 1 gives the time the birds spent with view on the mirror and shows how many bouts of close inspection of the mirror, of looks behind the mirror, of contingent behavior, and of social behavior were displayed by the birds. Three of the individuals (Gerti, Goldie, and Schatzi) spent a considerable amount of time in the compartment with the mirror, whereas the two other birds (Lilly and Harvey) appeared to avoid the compartment with the mirror. In the three birds with a preference for the mirror, behavior was characterized by close visual exploration of the mirror image (see Video S1 for an example). In addition, Gerti and Schatzi repeatedly looked behind the mirror and showed several bouts of behavior indicating contingency testing. Subjects moved their head or the whole body back and forth in front of the mirror in a systematic way (see Videos S2 and S3 for examples). In Goldie, contingent behavior was not demonstrated in this test, but demonstrated later in the mark test (see Video S4 ). Harvey and Lilly never showed any hint of such behavior. It is noteworthy that those birds that had a high interest in the mirror and also showed social displays only in the first tests were those that showed at least some evidence of self-directed behavior on later tests.

Mark Test

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 Video S6 for an example in the subject Schatzi). In the subsequent quantitative analysis, which compared the behavior in the mirror and mark condition with a condition without a mirror, mark-directed behavior (cf. Videos S5 and S7) in two of the birds, Gerti and Goldie, was significantly higher in the critical mirror and mark condition than in the other conditions. There were no instances in any of the birds of pecking at the reflection of the mark in the mirror. Figure 3 shows the quantitative amount of behavior towards the mark region as a proportion of all behaviors towards the own body for these two birds. Contrary to the absolute counts, this proportion will only increase with a specific effect on mark-directed behavior but not as a consequence of a possible overall increase in behaviors towards the own body. It can be seen that mark-directed behavior was only significantly enhanced when a mirror was present and the mark was colored and thus visible for the birds. The detailed frequencies in the different conditions are given in Table 2. The comparison of the frequencies of behaviors directed towards other parts of the body clearly shows that the mark-directed behaviors in the mirror and colored mark condition cannot be explained by a general increase of behavioral activity. A specific increase of mark-directed behavior in presence of a mirror is corroborated by the fact that mark-directed behavior ceased within trials as soon as the bird had removed the mark (see Video S8). In Figure 4A, performance of Gerti in a single test with change of marks is shown (see also Table 3). As this is only one test, findings should be interpreted with some caution, but consistent with the between-sessions comparison in the first test series, mark-directed behavior was high when the mark was visible in the mirror and low with the black control mark that was not visible. Figure 4B shows the results of an additional test with two sessions in the mirror and colored mark (yellow) condition and two control sessions with colored marks and a nonreflective plate instead of the mirror. Also in this case, mark-directed behavior only occurred with the mirror. With colored mark and mirror, over the two trials, there were five mark-directed actions per trial and 12 actions towards the rest of the body, whereas there was no mark-directed behavior at all when the bird wore a colored mark but no mirror was present. Again, findings clearly show that this significant difference cannot be explained by an unspecific increase in overall behavioral activity, as the overall rate of behaviors directed towards the own body was similar. These quantitative data are rather conservative as Gerti and Goldie removed the mark after a few minutes on most of the trials with a color mark and a mirror, and after removal of the mark, no mark-directed behaviors occurred (see Videos S5, S7, and S8 for different aspects of mark-directed behavior in the subject Gerti).

PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Figure 3. Proportion of Self-Directed Behavior towards the Mark Area Expressed as a Proportion of Overall Self-Directed Behavior in Subjects Gerti and Goldie 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 (p < 0.005, Fisher exact test), as well as in Goldie (p < 0.05, Fisher exact test), mark-directed behavior was significantly enhanced in the colored mark and mirror condition. https://doi.org/10.1371/journal.pbio.0060202.g003

PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Figure 4. Proportion of Self-Directed Behavior towards the Mark Area in Additional Tests (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 (p < 0.02, Fisher exact test). https://doi.org/10.1371/journal.pbio.0060202.g004

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 (Figure 3). It may well be that the black paper mark was slightly visible on the black plumage. This is supported by the observation that if the black mark condition elicited behavior, it was in the “mirror present” trials. This is an indirect support for the interpretation that the behavior towards the mark region was elicited by seeing the own body in the mirror in conjunction with an unusual spot on the own body.

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 Video S5). This is unlike chimpanzees, which, after discovering that the mark is inconsequential, rapidly lose interest [23]. The reason for the difference could be that bird's feathers are of considerably higher importance for survival than a patch of hair in chimps. This interpretation is supported by data showing that birds spend about one quarter of their resting time with preening and are often seen to interrupt sleeping in complete darkness only to preen [24].

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 Video S9), but not in the other. The subject Schatzi, which had shown spontaneous mark-directed behavior during an earlier exposure, showed no significant mark-directed behavior in this series of tests, although there were two instances of mark-directed behavior in the mirror and color condition and no mark-directed behavior in the other conditions.

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 [8,25]. Of 92 individuals tested by Povinelli et al. [8], only 21 demonstrated clear and nine weak evidence of self-exploration, with about 75% prevalence in young adults of 8 to 15 y. Only half among those with clear evidence of self-exploration passed the mark test. Thus, our data do not only qualitatively, but also quantitatively, match the findings in chimpanzees. As a note of caution, we would like, however, to emphasize that the number of birds we tested is too small for a definitive estimate of the distribution within the population. Thus, further studies must assess whether the typical frequency of mirror-induced self-directed behavior in magpies is comparable to that in chimpanzees.

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 [11]. Magpies are corvids, which belong to the order of Passeriformes, a phylogenetic group characterized by large brains relative to body weight [26]. The relative brain size of passeriform birds is similar to primates in allometric analyses, and within the Passeriformes, corvids stand out with particular high relative brain size [27]. Thus, magpies belong to a group of animals with very high relative brain size (see also Table 4).

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. [28] reported that prolonged operant conditioning of isolated components of the mark test in pigeons could produce a behavioral pattern that superficially looks like mirror-induced mark-directed behavior. This study could, however, not be replicated [29], and these authors also found reduction of self-directed behavior in pigeons in the conditions with a mirror, which strikingly contrasts with our findings in magpies. Additionally, extremely long periods of exposure to mirrors without specific training of self-related actions did not produce any kinds of behavior that was centered on the mark in monkeys [30,31]. Lastly, the mark test is only one piece of evidence of mirror-induced self-recognition in animals. Of equal importance are previous inspections of the mirror, such as during looks at the back side of the mirror, and exploration of mirror properties, such as during contingent behavior [1,8,10,32]. Our magpies showed self-related behavior in front of the mirror after a rather short cumulative exposure time and without being specifically trained to do so. In addition, when confronted with mirrors the first time, they displayed similar sequences of behavior as described in apes [1,2,3,8,32]. Although the mark test has been criticized [33,34], the main objections have been ruled out [23], and it remains one of the most useful tests for self-recognition in comparative studies [35]. When magpies are judged by the same criteria as primates, they show self-recognition and are on our side of the “cognitive Rubicon.” One should keep in mind that though mirror self-recognition reflects a crucial step in the emergence of self-recognition, the fully fledged capacity is complex, and comparative [36,37], clinical [38], and developmental studies [39] suggest an overall gradual development of this capacity.

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 [40] as well as their cognitive operations [17,41–43]. This high degree of evolutionary convergence is especially visible for the cognitive abilities of corvids and apes [17]. By demonstrating self-recognition in the mirror by magpies, the present study shows that even the neural capacity for distinguishing self and others has evolved independently in the two vertebrate classes and that a laminated cortex is not a prerequisite for self-recognition.