Anim Cogn (2015) 18:713–721 DOI 10.1007/s10071-015-0838-4 ORIGINAL PAPER Giant pandas failed to show mirror self-recognition Xiaozan Ma • Yuan Jin • Bo Luo • Guiquan Zhang • Rongping Wei • Dingzhen Liu Received: 16 July 2014 / Revised: 4 January 2015 / Accepted: 6 January 2015 / Published online: 22 January 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract Mirror self-recognition (MSR), i.e., the ability recognition in large mammals, provide new information on to recognize oneself in a mirror, is considered a potential a solitary species, and will be useful for enclosure design index of self-recognition and the foundation of individual and captive animal management. development. A wealth of literature on MSR is available for social animals, such as chimpanzees, Asian elephants Keywords Giant pandas Á Mirror self-recognition Á Age and dolphins, yet little is known about MSR in solitary difference Á Solitary animals Á Self-cognition mammalian species. We aimed to evaluate whether the giant panda can recognize itself in the mirror, and whether this capacity varies with age. Thirty-four captive giant Introduction pandas (F:M = 18:16; juveniles, sub-adults and adults) were subjected to four mirror tests: covered mirror tests, The ability to recognize oneself in a mirror, or mirror self- open mirror tests, water mark control tests, and mark tests. recognition (MSR), is an informative index of self-recog- The results showed that, though adult, sub-adult and nition and brain size (Liu and Yang 2009; Yang 2005). The juvenile pandas exposed to mirrors spent similar amounts MSR paradigm has been applied to evaluate self-awareness of time in social mirror-directed behaviors (v2 = 0.719, in a wide range of species (Gallup 1970, 1994; Sua´rez and P = 0.698), none of them used the mirror to touch the Gallup 1981), although this paradigm has been questioned mark on their head, a self-directed behavior suggesting by scientists (Heyes 1994, 1995). Previous research has MSR. Individuals of all age groups initially displayed shown that animals with relatively large brains have attacking, threatening, foot scraping and backwards walk- complex cognitive skills (Lefebvre et al. 2004) and are ing behaviors when exposed to their self-images in the likely to show MSR. The ability to recognize oneself in a mirror. Our data indicate that, regardless of age, the giant mirror is often assessed empirically by exposing animals pandas did not recognize their self-image in the mirror, but previously marked on the head (or elsewhere, in a position instead considered the image to be a conspecific. Our they can see only in a mirror) to a mirror, and assessing results add to the available information on mirror self- their behavior. Animals that possess MSR typically and progressively display four stages of behavior when they face a mirror: (1) non-mirror behaviors; (2) mirror-directed X. Ma Á Y. Jin Á D. Liu (&) behaviors; (3) mirror-guided behaviors; and (4) mark- Key Laboratory of Biodiversity Science and Ecological directed or self-directed behaviors (e.g., touching the mark Engineering of Ministry of Education, College of Life Sciences, on their body, thus demonstrating that they can see it and Beijing Normal University, Beijing 100875, China e-mail: [email protected] realize that it is on themselves) (Allen and Schwartz 2008; Plotnik et al. 2006). Since the pioneering work of Gallup B. Luo Á G. Zhang Á R. Wei (1970), who subjected four chimpanzees (Pan troglodytes) Key Laboratory for Reproduction and Conservation Genetics of to a MSR test, research has been published on MSR in Endangered Wildlife of Sichuan Province, China Conservation and Research Center for the Giant Panda, Wolong, Sichuan, human infants (Amsterdam 1972; Brooks-Gunn and Lewis China 1979; Mans et al. 1978), chimpanzees (Calhoun and 123 714 Anim Cogn (2015) 18:713–721 Thompson 1988; Lin et al. 1992) and orangutans (Pongo between panda-like eye-mask patterns that differ subtly in pygmaeus) (Lethmate and Du¨cker 1973). Although scien- shape (Dungl et al. 2008). These findings indicate that giant tists have tested for MSR in rhesus monkeys (Macaca pandas may have strong cognitive abilities. Typically, mulatta), java monkeys (M. fascicularis), stumptail maca- animals, including humans, which exhibit MSR, have lar- ques (M. speciosa), hamadryas baboons (Papio hama- ger relative brain sizes and more highly evolved social dryas), capuchin monkeys (Cebus paella), other lesser apes cognition abilities than those that show no MSR (Prior and pigeons (Columba liviadomestica), none of these spe- et al. 2008). Thus, the major aim of this study is to cies show sound evidence of MSR (Anderson 1984; investigate whether solitary giant pandas exhibit MSR. Anderson and Roeder 1989; de Waal et al. 2005; Gallup The development of self-recognition is correlated with and Suarez 1991; Mitchell and Anderson 1993; Shaffer and ontogeny and the development of other cognitive processes Renner 2000; Roma et al. 2007; Epstein et al. 1981; Toda (Gallup 1994). For example, human infants do not show and Watanabe 2008). The results of MSR studies in gorillas MSR until 18–24 months of age (Amsterdam 1972); in (Gorilla gorilla) are mixed (Allen and Schwartz 2008; chimpanzees, the age of onset of MSR appears to be Ledbetter and Basen 1982; Patterson and Cohn 2006). It is between 2 and 2.5 years of age (Lin et al. 1992), but either proposed that the results may be caused by cognitive bias a precipitous decline in self-recognition between 16 and due to the introduction of a new mirror image stimulus 20 years of age or a critical period effect in mid-life is (Keen et al. 2014) and the differences in enclosure/cage found in chimpanzees (Povinelli et al. 1993). Therefore, the structure, animal management and environmental enrich- second aim of this study is to explore the effect of age on ment for the subjects (Allen and Schwartz 2008); thus, the MSR in giant pandas. consistency and validity of MSR test protocols including To address these aims, we conducted a series of tests in environmental enrichment are key factors to produce reli- captive giant pandas. The results of this study may not only able and comparable results. Studies have shown that extend our understanding of MSR in animals with different bottlenose dolphins (Tursiops truncatus) (Reiss and Marino social structures, but also increase our knowledge of the 2001), Asian elephants (Elephas maximus) (Plotnik et al. cognitive ability of the giant panda. This knowledge can be 2006), and magpies (Pica pica) (Prior et al. 2008) also used to enhance the management and design of captive exhibit MSR, though some questions remain about the individuals’ enclosures and exhibits. evolution and adaptive value of MSR, and about the neu- rological processes involved (Suddendorf and Butler 2013). Materials and methods Most previous MSR studies were focused on social animals, and there is no published research on solitary Subjects and housing mammals. Solitary living animals will have less chance to encounter and interact with conspecifics in comparison Thirty-four giant pandas, ranging between 0.5 and 15 years with social living animals (Davies et al. 2012). However, of age and housed at the China Conservation and Research little is known whether solitary living animals have the Center for the Giant Panda, Bifengxia Base, Sichuan ability of MSR. Studies on MSR of solitary mammals Province, participated in the study. To study the effects of could throw light on the evolution of MSR, by showing age on MSR, subjects were divided into three groups: whether MSR is adaptive in solitary species. The giant adult, 5.5–15 years old; sub-adult, 1.5–5.5 years old; and panda (Ailuropoda melanoleuca) is an endangered solitary juvenile, 0.5–1.5 years old. Adults and sub-adults were species in China. Males and females communicate exten- individually maintained in enclosures consisting of an sively via scent and only occur together during the mating indoor bedroom (6 9 4 m) and an outdoor yard in an season (Schaller et al. 1985). They can identify each other irregular shape (about 100 9 60 m) with shrubs, herbs, through scent-markings (Liu et al. 2006; Swaisgood et al. climbing facilities and a small pond as the water source. 1999; Yuan et al. 2004; Zhang et al. 2008), vocalizations Their diet consisted of fresh bamboo, carrots, apples, and (Charlton et al. 2009) and cross-modal signaling (Xu et al. slices of savory panda bread (containing bamboo powder, 2012). In common with other bears, the giant panda has a soybean, and nutritional supplements). The juveniles were larger brain (relative to its body size) than other carnivore raised collectively in the panda baby center, which inclu- species (Gittleman 1986). It also has a larger Encephali- ded two enclosures each with an outdoor yard (30 9 20 m) zation Quotient (EQ) than the polar bear (Ursus maritimus) and an indoor cage (6 9 4 m). Test subjects were moved (EQJ: 0.961 vs 0.510 for the panda and polar bear, for the duration of the test to one of the indoor enclosures, respectively) (Dong and Zhang 2011). Research has shown while the other juveniles remained together in the other that giant pandas cannot only discriminate the colors red enclosure. The diet of juveniles consisted exclusively of and green (Kelling et al. 2006), but also differentiate formula milk (EnfamilÒ, Mead Johnson Nutritionals, 123 Anim Cogn (2015) 18:713–721 715 Evansville, Indiana; or EsblilacÒ, PetAgÒ, Hamsphire, cage, beyond the pandas’ reach (Fig. 1); for juveniles, the Illinois, USA) and bamboo shoots. Water was available ad mirror was placed about 30 cm away from the outside of lib to all subjects. the wire mesh fence.