Adult but not juvenile Barbary macaques spontaneou

Authors: Andrea Schell Kathrin Rieck Karina Schell Kurt Hammerschmidt Julia Fischer

Publish Date: 2011/02/12

Volume: 14, Issue: 4, Pages: 503-509

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Abstract

For groupliving animals it is crucial to distinguish one’s own group members from those of other groups Studies applying operant conditioning revealed that monkeys living in relatively small groups are able to recognize their own group members when tested with photographs of group members and other conspecifics Employing a simple looking time paradigm we here show that Barbary macaques living in two social groups comprising 46 and 57 individuals respectively at the enclosure ‘La Forêt des Singes’ at Rocamadour are able to spontaneously distinguish photographs of members of their own group from those depicting animals that belong to another group This ability appears to develop with age as juveniles did not discriminate between members of their own group and another group although they showed generally more interest in the pictures than did adults Juveniles frequently displayed picture directed behaviours such as lipsmacking touching and sniffing in both conditions indicating that the stimuli were highly salient to them In conclusion it appears that at least adult monkeys are able to memorize the faces of a large number of individuals Whether the difference in behaviour is based on individual recognition of one’s own group members or simply the discrimination based on familiarity remains unresolved However both mechanisms would be sufficient for group membership identificationIndividual recognition—the ability to store and retrieve from memory knowledge about specific individuals Shettleworth 2010—has been shown in a wide range of taxa reviewed in Tibbetts and Dale 2007 The recognition of the identity of others can be based on physical appearance vocalizations odours or a combination of cues Such recognition is a core requisite for the development of individualized relationships as well as the understanding of relationships between third parties Dasser 1988 Seyfarth and Cheney 1988 Bergman et al 2003In addition to recognizing others individually it is often crucial for socially living species to collectively distinguish one’s own group members from others There is evidence that nonhuman primates do not only distinguish between member of their own and other groups but that they also know where specific individuals are ranging Vervet monkeys Chlorocebus pygerythrus for instance responded more strongly to playbacks of intergroup ‘wrr’ vocalizations from a subject of a neighbouring group when this sound was presented from another territory than from the neighbouring group’s territory Cheney and Seyfarth 1982 This result indicates that the animals had come to associate a specific individual with its home range and knew the individuals’ voice characteristics Wild chimpanzees Pan troglodytes responded differentially to pant hoot vocalizations of group members neighbours and strangers Herbinger et al 2009 Groups of wild Barbary macaques Macaca sylvanus had more intense agonistic interactions with members of groups they rarely met compared to those they met frequently indicating that they remember and categorize individuals of different groups Deag 1971 This effect is known as the “dear enemy” effect and has also been found in birds Briefer et al 2008 as well as in lizards and ants Whiting 1999 Langen et al 2000 which were shown to respond more aggressively towards unfamiliar intruders compared to familiar neighbouring intruders but see Müller and Manser 2007While the adaptive value of individual recognition and discrimination of familiar individuals from less familiar ones is well established the outer limits of these abilities under natural conditions are less clear Due to methodological constraints we know to date much more about individual recognition in the auditory domain because calls can be easily played back to subjects Acoustic analyses revealed that a large number of vocalizations carry individual signatures Hammerschmidt and Todt 1995 Janik et al 2006 and playback studies showed that mother and infant in particular but also other individuals recognize each other based on such cues Fischer 2004 Charrier et al 2009 Kondo et al 2010 Sebe et al 2010Recognition of individuals in the visual domain has been predominantly studied in laboratory settings This research is closely linked to studies that investigated the fundamentals of face perception in nonhuman primates compared to humans Such studies revealed that humans and nonhuman primates appear to employ similar faceprocessing strategies Dahl et al 2009 The recognition of conspecific faces is based on holistic processing ie the face is processed as an unparsed whole Dahl et al 2010 Monkeys as well as humans categorize conspecific faces at the subordinate level of the individual individuation rather than at the basic level of the category ‘face’ Dufour et al 2006 Dahl et al 2007 The level of categorization however may depend on experience as monkeys were shown to be able to individuate members of other species using wholebody images after extended training Humphrey 1974A number of studies have examined whether monkeys distinguish between familiar and unfamiliar conspecific faces Pokorny and de Waal 2009b Marechal et al 2010 Chimpanzees categorize specific individuals using the concept of familiarity while matching pictures of faces of related individuals Parr et al 2000 Similarly dogs Canis familiaris Racca et al 2010 domestic cattle Bos taurus Coulon et al 2009 and crayfish Cherax destructor Van der Velden et al 2008 distinguish between different individuals as evidenced by preferential looking time paradigms and behavioural assays Using operant techniques such as matchtosample tasks it was shown that pigeons Columbia livia Wilkinson et al 2010 lemurs Eulemur fulvus and E macaco Marechal et al 2010 and capuchin monkeys Cebus apella Pokorny and de Waal 2009a b distinguish between familiar and unfamiliar conspecifics on the basis of photographic representationsOne limitation of instrumental settings is that subjects frequently receive extended training They are thus repeatedly exposed to pictures and are rewarded for correctly distinguishing between stimuli of the category in question Thompson and Oden 2000 and sometimes such procedures allow subjects to get accustomed to the pictures prior to the actual experiment Bovet and Vauclair 2000 Looking time paradigms such as preferential looking or habituationrecovery paradigms circumvent this problem yet they do not tell us much about the use of the cognitive abilities in question under more natural conditions Therefore complementary experiments in which subjects are not restrained are important to assess the evolutionary relevance of specific abilities

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