Head-shaking gestures are commonly used by African great apes to solicit activities such as play. Here, we report observations of head shaking in four bonobos apparently aimed at preventing the recipient from doing something. This may reflect a primitive precursor of the negatively connoted head-shaking behavior in humans. Further investigations are needed to clarify the preventive function of head shakes and their evolutionary role in the evolution of negation in humans

Call, Josep

Liebal, Katja

Schneider, C.

UEL Research Repository at University of East London

Do bonobos say NO by shaking their head? 1Running head: Do bonobos say NO by shaking their head? Word count: 2.497  Order of Authors: Christel Schneider; Josep Call; Katja Liebal Title: Do bonobos say NO by shaking their head? Christel Schneider1, Josep Call2, Katja Liebal1 1Freie Universität Berlin, Evolutionary Psychology, Berlin, GERMANY 2Max Planck Institute for Evolutionary Anthropology, Department of Developmental and Comparative Psychology, Leipzig, GERMANY  Electronic supplementary material: Video material is provided Do bonobos say NO by shaking their head? 2 1  2 Abstract Head shaking gestures are commonly used by African great apes to solicit 3 activities such as play.  Here, we report observations of head shaking in four bonobos 4 apparently aimed at preventing the recipient from doing something.  This may reflect a 5 primitive precursor of the negative connoted head shaking behaviour in humans.  Further 6 investigations are needed to clarify the preventive function of head shakes and their 7 evolutionary role in the evolution of negation in humans. 8  9  10 Keywords Communication; Gestures; Head shaking; Pan paniscus  11  12  13  14  15  16  17  18  19  20  21  22  23  24 Do bonobos say NO by shaking their head? 3Introduction 25 The head shake gesture (i.e., moving the head horizontally from side to side) is 26 regularly used as a communicative signal in humans.  Although head shaking can fulfil 27 several communicative functions, e.g., as a feedback signal during conversation (see 28 Cassell, 2000; McClave, 2000), it has been generally associated with an explicit or implicit 29 negative connotation in many parts of the world (Darwin, 1872; Morris, 1994; Kendon, 30 2002; cf., Darwin, 1872; Cassell, 2000, for cultural variations to this norm). 31 Head gestures have also been described in the African great apes, but not in 32 orangutans (e.g., van Lawick-Goodall, 1968; van Hooff, 1973; Becker, 1984; Tomasello et 33 al., 1997; Pika et al., 2003, 2005; Liebal et al., 2006; Tanner et al., 2006; Cartmill, 2008; 34 Genty et al., 2009).  More specifically, three main forms of head gestures have been 35 identified: bows (moving the torso and the head back and forth), nods (moving the head 36 vertically up and down) and shakes (moving the head horizontally from side to side).  37 Except for two isolated reports of chimpanzees signalling ‘no’ through head shaking 38 (Kortlandt, 1962; de Waal, 1982), head shakes in African great apes have been mainly 39 associated with an affiliative function, for instance, in the context of play (e.g., bonobos: 40 Pika, 2007; chimpanzees: van Hooff, 1973; gorillas: Tanner et al., 2006). 41 Here we report the first observations of head shakes in bonobos associated with 42 situations that are best described as preventing (or trying to prevent) another individual 43 from engaging (or re-engaging) in a certain activity.  The present study provides a 44 quantitative estimate of the prevalence and diversity of head gestures across all four ape 45 species and presents a detailed description of observed episodes of ‘preventive’ head 46 shaking in bonobos. 47  48 Do bonobos say NO by shaking their head? 4Methods  49  50 The reported observations were made during data collection for a research project 51 that focused on gestural acquisition in non-human great apes (Schneider, in preparation).  52 We videotaped 25 great ape infants during their first 20 months of life: six bonobos (Pan 53 paniscus), eight chimpanzees (Pan troglodytes), three gorillas (Gorilla gorilla), and eight 54 orangutans (Pongo pygmaeus).  The ape infants – housed in six European zoological parks 55 – were observed at different time periods, based on their age and their accessibility for 56 filming, between July 2001 and August 2008. 57 We videotaped the infants’ behaviour using focal animal sampling and scored all 58 communicative behaviour shown by the infant, as well as any signal directed towards the 59 infant by the mother or other group members.  In addition, all signals produced by the 60 mother and directed towards non-focal animals were also recorded whenever she was near 61 the infant and therefore in the view of the camera.  Overall, we obtained 190 hours of focal 62 animal observations (bonobos= 69h, chimpanzees= 79h, gorillas= 16h, orangutans= 26h). 63 We used a standardised and validated ethogram to score the communicative signals 64 (see Liebal et al., 2006 for definitions and criteria of communicative behaviour).  Three 65 forms of head gestures, as mentioned and defined in the introduction (bow, nod and shake), 66 were identified.  Additionally, we scored the following behavioural contexts in which the 67 gestures occurred: access, affiliation, agonism, grooming, ingestion, play, locomotion, 68 sexual and submission (see Liebal et al., 2006 for definitions). 69  70  71  72 Do bonobos say NO by shaking their head? 5Results 73  74  Both bonobos and chimpanzees made use of head gestures, whereas gorillas and 75 orangutans did not.  Bonobos displayed three head gestures; bow (n= 29), nod (n= 57), and 76 shake (n= 49), in nine distinct contexts: access, affiliation, agonism, grooming, ingestion, 77 play, locomotion, sexual and submission.  Chimpanzees, however, only displayed bow (n= 78 6) and nod (n= 16) gestures in two behavioural contexts: play and affiliation. 79 Of the 49 head shakes observed in bonobos, 13 occurred while trying to inhibit or 80 terminate a particular non-social behaviour of the recipient through active manipulation 81 (e.g., pulling back an infant that is running away).  These 13 ‘preventive’ instances 82 occurred during seven bouts of interactions and were primarily observed in mother-infant 83 dyads, with the mother and infant adopting the sender and recipient role, respectively (see 84 Table 1 for additional information).  However, in one instance an adult male showed a head 85 shake after the infant reached for the male’s food and in another instance a mother 86 employed head shaking after an adult female took food from her.  We recorded the 87 preventive signals in three behavioural contexts: affiliation, ingestion, and access (see 88 Liebal et al., 2006 for context definitions). 89 The signals were performed by four individuals living in three different captive 90 groups (the two communicators from Dierenpark Planckendael belonged to the same 91 group).  The mother-offspring dyad formed by Ulindi and Luiza produced a total of 16 head 92 shakes by the mother (ten preventive).  Yala produced eight head shakes (one preventive) 93 towards her offspring Kivu, while Kidogo and Djanoa only produced a single head shake in 94 their dyad (which was preventive in both cases).  In three of the seven interactions, one 95 head shake occurred; in three interactions two head shakes were performed, and in one 96 Do bonobos say NO by shaking their head? 6interaction four head shakes were displayed.  No other head gestures in bonobos or 97 chimpanzees were used with this preventive function.  To illustrate the use of the 98 preventive head shakes, here we provide a description of two of the observed episodes 99 (video recordings of these examples are available as electronic supplementary material). 100 Example 1 101 The mother and her female offspring were sitting next to each other on the ground.  102 The offspring started crawling away towards a nearby tree trunk and proceeded to 103 climb.  The mother retrieved the infant and positioned her back to her side.  The 104 infant made continual efforts to climb the trunk and each time the mother retrieved 105 her.  This culminated in the mother seizing the infant by the leg and shaking her 106 head while looking towards her.  The infant climbed once again, this time moving 107 around the tree (now out of sight of the mother).  After a while the mother got up, 108 moved around the tree, grabbed the infants’ arm and pulled her to the place where 109 they originally sat.  When releasing the infant the mother looked at her and shook 110 her head once more.  The mother started grooming another group member and the 111 infant moved towards the tree again. 112 Example 2 113 The mother and her female offspring were sitting next to each other on the ground 114 while the infant manipulated a piece of leek.  After a while, the mother took the 115 leek from the infant and threw it to the side.  Eventually the infant retrieved the 116 leek and the mother tried to recapture it.  The mother shook her head twice while 117 doing so and threw it away from her again.  The infant continued to move towards 118 the piece of leek. 119  120 Do bonobos say NO by shaking their head? 7Discussion 121 To date African great apes have been observed to display head shakes mainly for 122 initiating or resuming interactions such as play.  Here, we report the first observations of 123 head shakes in bonobos accompanying an active effort to terminate or prevent the recipient 124 from engaging in a particular behaviour.  Although we observed head gestures in both 125 chimpanzees and bonobos, only the latter employed head shakes (cf., van Hooff, 1973; 126 Tomasello et al., 1997; Liebal et al., 2004).  Moreover, bonobos produced head shaking for 127 initiating, maintaining and terminating interactions, and in general they used head gestures 128 more frequently than chimpanzees and in a greater variety of contexts.  These findings 129 indicate that bonobos are more sophisticated in their use of the head as a signal medium 130 when compared with the other ape species. 131 One possible explanation for bonobos’ extensive variety of head gestures might 132 stem from their higher levels of inter-individual tolerance and diffused hierarchical 133 structures (Paoli et al., 2006; Hare et al., 2007).  For example, according to the ‘emotional 134 reactivity hypothesis’ (Hare & Tomasello, 2005), bonobos differ from other apes in their 135 social-problem solving strategies because their emotional temperament affords more 136 cooperative behaviour.  In relation to this, Maestripieri (1999) proposed that species living 137 in egalitarian-individualised societies, with diffused hierarchical structures, are more likely 138 to develop greater sophistication in their communicational systems than despotic societies 139 who have strict hierarchies.  In this regard, bonobos might have developed 140 communicational signals such as the preventive head shake to coordinate, and possibly 141 negotiate, during situations of conflict. 142 Nevertheless, additional research is required.  Single-case observations of head 143 shaking with a negative connotation have been reported in chimpanzees (Kortlandt, 1962; 144 Do bonobos say NO by shaking their head? 8de Waal, 1982).  Future research using a more systematic, cross-species approach could 145 clarify whether our observed inter-species differences were due to small sample sizes or 146 observation times.  Furthermore, more detailed studies are needed to establish the 147 functional role of all forms of head gestures (e.g., shake, nod, bow) for each species. 148 Current research on gestural communication in great apes has shown that the use of 149 the head as a communication device is more prevalent in African apes compared to 150 orangutans and other primates (Becker, 1984; Liebal et al., 2006; Cartmill, 2008).  151 Although some monkeys possess well-defined head gestures (e.g., head flagging in gray-152 cheeked mangabeys; Wallis, 1983), they appear more stereotyped and less diverse than 153 those observed in African great apes.  Calling attention to the preventive communicative 154 function of a previously described gesture contributes to expand the variety of motives 155 underlying gestural use in the great apes.  Until now, most great ape gestures, not just head 156 gestures, have been interpreted as invitations to engage in various activities or as 157 announcements of impending behaviour (Call & Tomasello, 2007).  It is true that some 158 intention movements can inform recipients about the actor’s intent to prevent some activity.  159 For instance a dominant animal can take a step in the direction of an object to inform others 160 about its intent to claim it, and thus preventing others from taking it.  However, this is quite 161 different from the head shaking gesture which, by itself, does not indicate any particular 162 action.  If the use of preventive head shaking is confirmed in genus Pan, this would raise a 163 further, more speculative, evolutionary question: Do these gestures reflect a primitive 164 precursor of the human head shake that denotes negation?  This is an intriguing possibility 165 but additional data along the lines indicated above will be needed to be able to provide an 166 informed answer. 167  168 Do bonobos say NO by shaking their head? 9 169  170 Acknowledgements We thank Dierenpark Planckendael (Belgium), Leipzig Zoo, Berlin 171 Zoo, and Muenster Zoo (Germany), as well as Apenheul and Arnhem Zoo (Holland) for 172 allowing us to conduct our research.  For fruitful discussions and comments on earlier 173 drafts of this manuscript, we thank M. Chase, H. Gretscher, and M. Halina.  Thanks to the 174 anonymous reviewers for their helpful comments.  This study is part of the interdisciplinary 175 research project “Towards a grammar of gesture” which is funded by the Volkswagen 176 Foundation (Hannover, Germany). 177  178  179  180  181  182  183  184  185  186  187  188  189  190  191  192 Do bonobos say NO by shaking their head? 10References 193 Becker C (1984) Orang-Utans und Bonobos im Spiel: Untersuchungen zum Spielverhalten 194 von Menschenaffen. Profil-Verlag, München 195 Call J,Tomasello M (2007) The Gestural Communication of Apes and Monkeys. Lawrence 196 Erlbaum Associates, New Jersey 197 Cartmill EA (2008) Gestural Communication in Orangutans (Pongo pygmaeus and Pongo 198 abelii): A Cognitive Approach. University of St Andrews, St Andrews 199 Cassell J (2000) Nudge Nudge Wink Wink: Elements of Face-to-Face Conversation for 200 Embodied Conversational Agents. In Cassell J, Sullivan JW, Prevost S & Churchill 201 EF (eds), Embodied Conversational Agents. 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Int J Primatol 4: 153-166 255  256  257  258  259  260  261  262  263 264 Do bonobos say NO by shaking their head? 13 265 Tables 266  267 Table 1   Number of preventive head shakes corresponding to dyad, location and context of interaction bout. Location Sender-recipient dyad  Number of head shakes per interaction bout Context Leipzig Zoo Mother → Offspring Ulindi        Luiza 2 Affiliation a 2 Affiliation 2 Access b 4 Ingestion Dierenpark Planckendael Adult male → Infant Kidogo            Habari 1 Ingestion Mother → Adult Female Djanoa     Hortense 1 Ingestion Berlin Zoo Mother → Offspring Yala           Kivu 1 Affiliation aSee Example 1 in text.  bSee Example 2 in text.  268 

Do bonobos say NO by shaking their head?

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Do bonobos say NO by shaking their head?

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