James R. Anderson

Mirror self-recognition: a review and critique of attempts to promote and engineer self-recognition in primates

We review research on reactions to mirrors and self-recognition in nonhuman primates, focusing on methodological issues. Starting with the initial demonstration in chimpanzees in 1970 and subsequent attempts to extend this to other species, self-recognition in great apes is discussed with emphasis on spontaneous manifestations of mirror-guided self-exploration as well as spontaneous use of the mirror to investigate foreign marks on otherwise nonvisible body parts—the mark test. Attempts to show self-recognition in other primates are examined with particular reference to the lack of convincing examples of spontaneous mirror-guided self-exploration, and efforts to engineer positive mark test responses by modifying the test or using conditioning techniques. Despite intensive efforts to demonstrate self-recognition in other primates, we conclude that to date there is no compelling evidence that prosimians, monkeys, or lesser apes—gibbons and siamangs—are capable of mirror self-recognition.

Third-party social evaluations of humans by monkeys and dogs

HighlightsCapuchin monkeys negatively evaluate people who refuse to help a third party.Capuchin monkeys negatively evaluate people who exchange unfairly with others.Dogs negatively evaluate people who refuse to help their owners.Nonhuman species can engage in third‐party based social evaluations. Abstract Developmental psychologists are increasingly interested in young children’s evaluations of individuals based on third‐party interactions. Studies have shown that infants react negatively to agents who display harmful intentions toward others, and to those who behave unfairly. We describe experimental studies of capuchin monkeys’ and pet dogs’ differential reactions to people who are helpful or unhelpful in third‐party contexts, and monkeys’ responses to people who behave unfairly in exchanges of objects with a third party. We also present evidence that capuchin monkeys monitor the context of failures to help and violations of reciprocity, and that intentionality is one factor underlying their social evaluations of individuals whom they see interacting with others. We conclude by proposing some questions for studies of nonhuman species’ third party‐based social evaluations.

Evaluation of third-party reciprocity by squirrel monkeys (Saimiri sciureus) and the question of mechanisms

Social evaluation during third-party interactions emerges early in human ontogeny, and it has been shown in adult capuchin monkeys who witness violations of reciprocity in object exchanges: Monkeys were less inclined to accept food from humans who refused to reciprocate with another human. A recent study reporting similar evidence in marmoset monkeys raised the possibility that such evaluations might be based on species’ inherent cooperativeness. We tested a species not renowned for cooperativeness—squirrel monkeys—using the procedure used with marmosets and found a similar result. This finding rules out any crucial role for cooperative tendencies in monkeys’ responses to unfair exchanges. We then tested squirrel monkeys using procedures more similar to those used in the original study with capuchins. Squirrel monkeys again accepted food less frequently from non-reciprocators, but unlike capuchins, they also strongly preferred reciprocators. We conclude that neither squirrel monkeys nor marmoset monkeys engaged in emotional bookkeeping of the type that probably underlies social evaluation in capuchin monkeys; instead, they employed one or more simple behavioral rules. Further comparative studies are required to clarify the mechanisms underlying social evaluation processes across species.

Chimpanzees and death

Information about responses to death in nonhuman primates is important for evolutionary thanatology. This paper reviews the major causes of death in chimpanzees, and how these apes respond to cues related to dying and death. Topics covered include disease, human activities, predation, accidents and intra-species aggression and cannibalism. Chimpanzees also kill and sometimes eat other species. It is argued that, given their cognitive abilities, their experiences of death in conspecifics and other species are likely to equip chimpanzees with an understanding of death as cessation of function and irreversible. Whether they might understand that death is inevitable—including their own death, and biological causes of death is also discussed. As well as gathering more fundamental information about responses to dying and death, researchers should pay attention to possible cultural variations in how great apes deal with death. This article is part of the theme issue ‘Evolutionary thanatology: impacts of the dead on the living in humans and other animals’.

The “olfactory mirror” and other recent attempts to demonstrate self-recognition in non-primate species

The recent attempt by Horowitz (2017) to develop an olfactory mirror test of self-recognition in domestic dogs raises some important questions about the kinds of data that are required to provide definitive evidence for self-recognition in dogs and other species. We conclude that the olfactory mirror constitutes a compelling analog to the mark test for mirror self-recognition in primates, but despite claims to the contrary neither dogs, elephants, dolphins, magpies, horses, manta rays, squid, nor ants have shown compelling, reproducible evidence for self-recognition in any modality.

Reflections in the rainforest: full-length mirrors facilitate behavioral observations of unhabituated, wild chimpanzees

We describe behaviors of unhabituated wild chimpanzees in Gabon during repeated encounters with large mirrors installed permanently in their home range. Movement in proximity to the mirrors triggered video cameras that recorded the scene. Data are presented for 51 mirror encounters spanning a 3-year period. After initial wariness, mirror-directed aggressive behaviors were common, especially in adult males, but aggression gradually diminished and eventually almost completely ceased. Focusing on the two mirrors that elicited most reactions, the percentage of chimpanzees showing tension or anxiety also decreased across encounters. These mirrors elicited a range of socio-sexual behaviors interpreted as having a reassurance function, especially when group-level tension appeared high. Chimpanzees also occasionally directed these behaviors towards their own reflection. Despite increasing habituation and positive attraction to the mirrors, none of the chimpanzees displayed signs of self-recognition. We conclude that a combination of large mirrors and video traps can provide valuable information about unhabituated, semi-terrestrial primates in their natural habitat, by inducing the primates to stay in one place for longer than they might otherwise do.

Factors influencing deceptive behaviours in Tonkean macaques (Macaca tonkeana)

The complex social environments of primates create opportunities for engaging in tactical deception, especially for subordinate individuals. We analysed the behaviour of subordinate Tonkean macaques with dominant conspecifics in an experimental food competition context. The subordinate macaque could see two pieces of food in a test area, but only one piece was visible to the dominant. Both individuals were released into the test area at the same time or with the subordinate given a short head start on the dominant. Here, based on video analysis of the subordinates’ behaviours, we describe and classify functionally deceptive behaviours displayed by subordinates, and report factors that influenced these behaviours. Subordinates used several types of tactical deception, including concealment and distraction, especially when paired with competitors of much higher social rank, and they obtained the hidden food more frequently when they used a combination of tactics rather than only one.

Editorial to the special feature: Franco-Japanese collaboration in primatology

Like most other fields of science and technology (Wagner 2006), primatology has seen rapid and continuing growth in studies conducted by multiple researchers working collaboratively, both in situ and by data sharing and correspondence. A recently published paper describing one aspect of behavior in wild chimpanzees has 80 authors based in ten different countries! The absolute and relative number of multi-authored papers on primates has risen massively since the early days of primate research. A quick comparison of the contents of the earliest and the most recent volumes of Primates illustrates this change. The two issues of volume 1 (published 1957–1958) contain 15 articles, every one written by a single author, of which 14 are Japanese and one is non-Japanese. By contrast, the four issues of the most recent volume (vol. 56, 2015) contain 40 articles (including ‘‘News and Perspectives’’), of which only seven (17.5 %) are single-author papers. A closer look reveals the increasing impact of international collaborations on our discipline. Of the 33 jointly authored papers in Primates vol. 56, thirteen (39 %) list authors from institutions within the same country. More striking is the fact that 20 papers (61 %) have authors who are based in institutions in different countries. Japanese primatologists are well represented in these international efforts, with 30 % of these papers including at least one author based in a Japanese institution. The sharing of ideas, information and observations between Japanese primatologists and their colleagues from other nations goes back to at least the early 1960s. The Japan-India Joint Project in Primates Investigation led to the first publication on primates co-authored by scientists based in Japan and another nation (Sugiyama et al. 1965). Several authors have discussed how bi-directional visits and interactions, starting in the 1950s, and more recently joint research projects, have impacted both on western and Japanese primatology (Asquith 2000; de Waal 2003; Matsuzawa and McGrew 2008). This issue of Primates includes several papers that highlight collaborative projects between Japanese researchers and colleagues from the francophone primatological community. It is just over 400 years since a Japanese samurai and ambassador initiated contacts between Japan and France. Since then there has been a long series of diplomatic, industrial, cultural and scientific exchanges between the two countries that continues today. In this context it is worth briefly mentioning some aspects of the history of primatology in the two countries. Japan, of course, has its own indigenous nonhuman primate population; although France has none, many of its former colonies in Africa and Asia contain diverse species of primates, and these have long attracted the attention of Japanese primatologists. Chimpanzees at Bossou, studied almost continuously by Japanese primatologists since 1976, were actually described decades earlier by the French naturalist Maxime Lamotte, when Guinea was still a French colony. However, it would be more than five decades before the publication of an article jointly authored by Japanese and French scientists concerning Bossou. The Primate Society of Japan (PSJ) was established in 1985, & James Anderson jra6655@googlemail.com

Tending a dying adult in a wild multi-level primate society

Responses of nonhuman species to dying and dead conspecifics range from hard-wired, fixed-action patterns - as in social insects - to varied, flexible behaviors with cognitive and emotional correlates - as in some larger-brained mammals [1,2]. Comparative thanatology addresses issues that include empathy, compassion, and conceptual understanding of death across species [1-3]. Several aspects of how great apes react to illness, injury and death of others recall human behavior in comparable situations [1-5]. However, the extent to which more distantly related primates share these responses is largely unknown. Here, we describe behaviors shown toward a dying adult female in wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) [6] and argue that empathy and compassion surrounding death extend beyond humans and their closest evolutionary relatives.

Observational learning in capuchin monkeys: a video deficit effect

Young human children have been shown to learn less effectively from video or televised images than from real-life demonstrations. Although nonhuman primates respond to and can learn from video images, there is a lack of direct comparisons of task acquisition from video and live demonstrations. To address this gap in knowledge, we presented capuchin monkeys with video clips of a human demonstrator explicitly hiding food under one of two containers. The clips were presented at normal, faster than normal, or slower than normal speed, and then the monkeys were allowed to choose between the real containers. Even after 55 sessions and hundreds of video demonstration trials the monkeys’ performances indicated no mastery of the task, and there was no effect of video speed. When given live demonstrations of the hiding act, the monkeys’ performances were vastly improved. Upon subsequent return to video demonstrations, performances declined to pre-live-demonstration levels, but this time with evidence for an advantage of fast video demonstrations. Demonstration action speed may be one aspect of images that influence nonhuman primates’ ability to learn from video images, an ability that in monkeys, as in young children, appears limited compared to learning from live models.