Azure-winged magpies fail to understand the principle of mirror imaging
Introduction
The mirror self-recognition (MSR) paradigm has emerged as a standard method for evaluating self-awareness in many species since the pioneering work by Gallup (Gallup, 1970), although numerous researchers have debated whether animals that show MSR possess human-like self-awareness (Heyes, 1994, 1995; Bard et al., 2006). The ability to recognise oneself in a mirror is rare in the animal kingdom. Most of the animals exposed to the mirror test displayed various social behaviours (such as aggressive behaviour) and continued to do so during repeated testing (Prior et al., 2008). The ability to recognise oneself in a mirror is often assessed empirically by exposing animals (previously marked on the head or elsewhere on a spot they can see only in the mirror) to a mirror and assessing their behaviour. If the tested animals respond with mark-directed or self-directed behaviours (e.g. touching the mark on their body, demonstrating that they can see it and realise that the mark it is on themselves) after exposure to the mirror, then the animal passes the mirror-mark test (Ma et al., 2015).
Fairly clear evidence of self-recognition has been obtained in some non-human primate species, although mirror-directed behaviour is much less stable in these species than in human (Swartz and Evans, 1991; Povinelli et al., 1993). Some studies have provided clear evidence of self-awareness in chimpanzees (Pan troglodytes)(Gallup, 1970), orangutans (Pongo pygmaeus) (Lethmate and Dücker, 1973) and bonobos (P. paniscus) (Walraven et al., 1995). A few gorillas (Gorilla gorilla) (Ledbetter and Basen, 1982; Hyatt, 1998; Posada and Colell, 2007) have shown MSR, although the findings are less robust than those reported for other ape species. Also, video evidence showing compelling self-recognition in gorillas is markedly lacking. No strong evidence exists to show that gibbons (Hylobates lar), siamangs (H. syndactylus) (Anderson and Gallup, 2015) and other primates are capable of self-recognition (Ujhelyi et al., 2000). An exhaustive review of the existing self-recognition literature on primates has been conducted by Anderson and Gallup (2015). Furthermore, some non-primates have shown mark-directed performance in the same mark test taken by primates. One Bottlenose dolphins (Tursiops truncates) (Reiss and Marino, 2001), one Asian elephant (Elephas maximus) (Plotnik et al., 2006), two Eurasian magpies (Pica pica) (Prior et al., 2008) and four Indian house crows (Corvus splendens) (Buniyaadi et al., 2019) have reportedly passed the mark test.
As it has been clearly shown that higher cognitive abilities are not restricted to the brains of primates, some novel self-recognition studies have moved beyond just phylogenetic causes to focus on ecological explanations. Horowitz (2017) has recently claimed the approximation of self-recognition in dogs using an ‘olfactory mirror’, i.e. the dog’s own urine. Horowitz’s study translates the MSR study for dogs (who primarily rely on olfaction) who have shown interest in their own odours, implying the dogs’ recognition of the odour that came from them. Gallup and Anderson (2018) have reported their critique of the olfactory mirror with dogs. A task exploiting an ecologically relevant behaviour has been used to assess the self-recognition of Clark’s nutcrackers (Nucifraga columbiana) (Clary and Kelly, 2016) and California scrub jays (Aphelocoma californica) (Clary et al., 2019). When presented with a blurry, rather than clear mirror, Clark’s nutcrackers show more mark-directed behaviours and cache more often, suggesting that they interpret the blurry image as their own rather than a conspecific. These tested California scrub jays do not show increased caching and cache protection behaviours in the presence of a mirror and no mark-directed behaviours in the mark test.
Numerous studies have reported that animals that do not conclusively pass the mark test show other interesting and intermediate mirror-induced responses, such as mirror-triggered search and peekaboo (Gallup, 1970; Anderson, 1984; Pepperberg et al., 1995; Suddendorf and Collier-Baker, 2009). Mirror-triggered search is a basic task for exploring whether animals can find hidden food (that is visible in the mirror but invisible directly) using the mirror as a cue (Menzel et al., 1985; Anderson, 1986; Povinelli, 1989). Animals can find hidden food at a fixed location by exploiting the correlation between an object and its reflection; however, they do not need to understand that the object is being reflected by the mirror or that the mirror is used to guide their actions (Pepperberg et al., 1995).Contrarily, the mirror-mediated spatial location task requires a highly complicated cognitive competence (Menzel et al., 1985; Anderson, 1986; Povinelli, 1989; Pepperberg et al., 1995) because the subjects must use the mirror without any trial and error attempts to find the reward hidden in one of several locations. Subjects must understand the correspondence between the location of the reward in real space and the information in mirror. A study in 2011 demonstrated that New Caledonian crows (C. moneduloides) learnt to associate a mirror image of meat with finding the bait in its actual location (Medina et al., 2011). Macaques (Macaca fuscata) can use a mirror to reach hidden food that is only visible with a mirror. In addition, a more elaborative mirror-guided reaching task (Menzel et al., 1985; Anderson, 1986) was designed to test whether animals could synchronise mirrors with their own body movements.
Previous studies have suggested that some bird species have evolved highly cognitive skills similar to those of humans and apes (Lefebvre et al., 2002; Deregnaucourt and Bovet, 2016). These skills are manifested by these birds by completing different tasks, such as using tools and predicting the behaviour of conspecifics using their episodic-like memory and own experience (Duffey, 1993; Emery and Clayton, 2004). Mirror-directed behaviour has been studied in different species of birds, both in the wild (e.g. chickadees (Parus atricapillus) (Censky and Ficken, 1982) and glaucous-winged gulls (Larus glaucescens) (Stout, 1969)) and in the laboratory (e.g. blue grouse (Dendragapus obscurus) (Stirling, 1968), budgerigars (Melopsittacus undulates) (Gallup and Capper, 1970), African grey parrots (Psittacus erithacus) (Pepperberg et al., 1995), New Caledonian crows (Medina et al., 2011), jungle crows (C. macrorhynchos) (Kusayama et al., 2000) and jackdaws (C. monedula) (Soler et al., 2014)). Most of these birds have responded to their self-image in the mirror with different social behaviours, i.e. treating the mirror image as if viewing a conspecific, exhibiting aggressive behaviour and exhibiting displays of courtship. A flock of flamingos (Phoeniconais minor) has displayed a very interesting behaviour of marching in front of the mirror (Pickering and Duverge, 1992).
Several corvid species have been subjected to mirror tests and displayed a range of different reactions to the mirror. The studies on captive jungle and New Caledonian crows have revealed that these crows consider their mirror images as their conspecifics and show no self-recognition behaviour in the mirror-exposure test (Kusayama et al., 2000; Medina et al., 2011). Carrion (C. corone) and hooded crows (C. cornix) exhibit exploratory behaviours rather than social behaviours on their first encounters with a mirror, but none of the crows show significant mark-directed behaviours (Vanhooland et al., 2019). Surprisingly, two out of five Eurasian magpies have passed the mark test after cumulative exposure to mirrors (Prior et al., 2008). Thereafter, four of six Indian house crows have been reported to have the ability of self-recognition in a study that followed a procedure similar to the one described in the Eurasian magpie study (Prior et al., 2008; Buniyaadi et al., 2019). A recent study has shown that jackdaws fail the mark test (Soler et al., 2014). They show a mark-directed behaviour in the mirror that is similar to their behaviour without a mirror. Researchers hypothesise that the magpies and the jackdaws may have detected the mark by tactile sense. Meanwhile, researchers also suggest the adoption of appropriate marking methods in future marking tests, such as paint that does not agglomerate the feathers.
Azure-winged magpies (Cyanopica cyana), a corvid species attracted lots of attention from researchers, are found in Eastern Asia (Yamagishi and Fujioka, 2007; Ren et al., 2016; Wang et al., 2019). The corvid species was the first to experimentally show proactive pro-sociality, which is considered a human hallmark (Horn et al., 2016). MSR is thought to correlate with higher forms of empathy and altruistic behaviour. We inferred that azure-winged magpies would be good candidates for mirror test because of their proactive pro-sociality. In this study, we tested and observed the responses of seven hand-raised azure-winged magpies to mirrors through four tests. (1) Mirror preference and standardised mirror exploration (Test 1): In this test, we assessed the preference for mirrors and the quantified mirror-directed behaviours of the subjects. (2) Single vertical mirror test (Test 2): We investigated the mirror-directed behaviours of each subject. (3) Mark test (Test 3): Each subject was marked (in the throat area) to explore whether a mark-directed behaviour in front of the mirror would be exhibited. (4) Mirror-triggered search test (Test 4): This test was used to investigate whether the subjects would learn to use the mirror to find hidden food. Similar to the experimental procedure of the study on European magpies (Prior et al., 2008), the first three tests were conducted to investigate whether azure-winged magpies would show MSR. Most of the subjects were unwilling to approach the experimental cages because of neophobia. Therefore, their home and experimental cages were connected to eliminate their fear and encourage them to display their behaviour in their normal state.
Section snippets
Subjects
Seven azure-winged magpies (named Daniel, Emily, Fatty, Joyce, Tiny, Alina and Neil) served as the subjects throughout the study. The subjects were suitable for the study because they had not encountered mirrors before. The magpies were housed in a seven-cage indoor aviary. All cages were provided with perching space, branches and cribs. The subjects were in auditory and visual contact with their conspecies before the experimental procedures began, but they were single-housed in home cages. All
Mirror preference and standardised mirror exploration (Test 1)
Seven subjects participated in five sessions of Test 1 on separate days. The apparatus of the experimental cage was invisible directly, so several of the subjects were unwilling to enter the experimental cage because of neophobia. Four subjects stayed in their home cages throughout the five sessions. Finally, only three of the seven birds entered the experimental cage. Each bird underwent five consecutive trials for approximately 30 ± 7.74 min. on separate days.
The durations in the experimental
Discussions
Upon exposure to a mirror for the first time, animals commonly respond in one of three ways. (1) They regard their image in the mirror as a conspecific or another animal, thus exhibiting different social behaviours (such as aggressive and submissive behaviours) towards it or looking behind the mirror to search for the conspecific. (2) They perceive their mirror images as illusory and ignore them, showing interest only in the smooth surface (Ma et al., 2015). (3) They recognise themselves in the
Declaration of Competing Interest
The authors declare that they have no conflict of interest.
Ethical standards
The study was conducted according to the Ethics Review Committee of Nanjing University (No. 2009-116). All applicable international, national and institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants.
Author contributions
LW, YL, ZL designed the study, LW, YL, HW, YZ, HY did the experiments, LW, YL, ZL analyzed the data, LW drafted the manuscript, SU and ZL reviewed and polished the manuscript.
Acknowledgement
This work was supported by National Natural Science Foundation of China (No. 31772470, J1210026).We thank Professor Cheng Huang for special venue support, Kaibao Wang for statistical advice, Chunhong Liu, Hui Fang, Yanning Qiu and Zhiyu Zhou for taking care of the birds.
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