Abstract
Reading the attentional state of an audience is crucial for effective intentional communication. This study investigates how individual learning experience affects subsequent ability to tailor gestural communication to audience visual attention. Olive baboons were atypically trained to request food with gestures by a human standing in profile, while not having access to her face. They were tested immediately after training, and then 1 year later in conditions that varied the human’s cues to attention. In immediate testing, these baboons (profile group baboons) gestured towards untrained cues regardless of their relevance for visual communication. They were also less discriminant towards trained versus untrained cues than baboons trained by a human facing them (face group baboons, tested in Bourjade et al. Anim Behav 87:121–128; Bourjade et al., Anim Behav 87:121–128, 2014). In delayed testing, the number of gestures towards meaningful untrained cues increased and profile group baboons discriminated the orientation of the human body, a conspicuous proxy of visual attention. Our results provide support for the primary interplay between implicit learning and systematically reinforced associations made through explicit training in the scaffolding of intentional gesturing tuned to audience attention.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson J, Kuwahata H, Fujita K (2007) Gaze alternation during “pointing” by squirrel monkeys (Saimiri sciureus)? Anim Cogn 10:267–271. https://doi.org/10.1007/s10071-006-0065-0
Bard KA, Leavens DA (2014) The importance of development for comparative primatology. Annu Rev Anthropol 43:183
Bard KA, Bakeman R, Boysen ST, Leavens DA (2014) Emotional engagements predict and enhance social cognition in young chimpanzees. Dev Sci 17:682–696
Barrera G, Mustaca A, Bentosela M (2011) Communication between domestic dogs and humans: effects of shelter housing upon the gaze to the human. Anim Cogn 14:727–734
Bates E, Camaioni L, Volterra V (1975) The acquisition of performatives prior to speech. Merrill-Palmer Q 21:205–226
Bentosela M, Barrera G, Jakovcevic A et al (2008) Effect of reinforcement, reinforcer omission and extinction on a communicative response in domestic dogs (Canis familiaris). Behav Process 78:464–469
Bourjade M (2016) Le pointage controversé des singes: éléments empiriques chez le babouin olive. Enfance, 2016(4), 375–404
Bourjade M (2017) Social attention. In: Fuentes A (ed) The international encyclopedia of primatology. Wiley, New York
Bourjade M, Meguerditchian A, Maille A et al (2014) Olive baboons, Papio anubis, adjust their visual and auditory intentional gestures to the visual attention of others. Anim Behav 87:121–128. https://doi.org/10.1016/j.anbehav.2013.10.019
Bourjade M, Canteloup C, Meguerditchian A et al (2015) Training experience in gestures affects the display of social gaze in baboons’ communication with a human. Anim Cogn 18:239–250
Brown H, Prescott R (2006) Applied mixed models in medicine. Wiley, Hoboekn
Bruner JS (1975) The ontogenesis of speech acts. J Child Lang 2:1–19
Bulloch MJ, Boysen ST, Furlong EE (2008) Visual attention and its relation to knowledge states in chimpanzees, Pan troglodytes. Anim Behav 76:1147–1155
Burnham KP, Anderson DR (2004) Multimodel inference understanding AIC and BIC in model selection. Soc Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644
Butterworth G (2004) Joint visual attention in infancy. In: Bremner G, Fogel A (eds) Blackwell handbook of infant development. Blackwell, Hoboken pp 213–240
Canteloup C, Bovet D, Meunier H (2015) Do Tonkean macaques (Macaca tonkeana) tailor their gestural and visual signals to fit the attentional states of a human partner? Anim Cogn 18:451–461
Carpenter M, Nagell K, Tomasello M et al (1998) Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monogr Soc Res Child Dev 63:1–174. https://doi.org/10.2307/1166214
Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348. https://doi.org/10.1016/j.cub.2007.06.069
Elgier AM, Jakovcevic A, Mustaca AE, Bentosela M (2009) Learning and owner–stranger effects on interspecific communication in domestic dogs (Canis familiaris). Behav Process 81:44–49
Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. https://doi.org/10.1016/S0149-7634(00)00025-7
Franco F, Butterworth G (1996) Pointing and social awareness: declaring and requesting in the second year. J Child Lang 23:307–336. https://doi.org/10.1017/S0305000900008813
Frank LK (1926) The problem of learning. Psychol Rev 33:329–351. https://doi.org/10.1037/h0074050
Frischen A, Bayliss AP, Tipper SP (2007) Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychol Bull 133:694
Gaunet F, Massioui FE (2014) Marked referential communicative behaviours, but no differentiation of the “knowledge state” of humans in untrained pet dogs versus 1-year-old infants. Anim Cogn 17:1137–1147. https://doi.org/10.1007/s10071-014-0746-z
Genty E, Byrne R (2010) Why do gorillas make sequences of gestures? Anim Cogn 13:287–301. https://doi.org/10.1007/s10071-009-0266-4
Genty E, Zuberbühler K (2014) Spatial reference in a bonobo gesture. Curr Biol 24:1601–1605
Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn 12:527–546. https://doi.org/10.1007/s10071-009-0213-4
Gómez JC (2005a) Requesting gestures in captive monkeys and apes: Conditioned responses or referential behaviours? Gesture 5:91–105. https://doi.org/10.1075/gest.5.1.08gom
Gómez J-C (2005b) Species comparative studies and cognitive development. Trends Cogn Sci 9:118–125. https://doi.org/10.1016/j.tics.2005.01.004
Gómez J-C (2007) Pointing behaviors in apes and human infants: a balanced interpretation. Child Dev 78:729–734. https://doi.org/10.1111/j.1467-8624.2007.01027.x
Guo K, Robertson RG, Mahmoodi S et al (2003) How do monkeys view faces?—a study of eye movements. Exp Brain Res 150:363–374
Hattori Y, Kuroshima H, Fujita K (2010) Tufted capuchin monkeys (Cebus apella) show understanding of human attentional states when requesting food held by a human. Anim Cogn 13:87–92. https://doi.org/10.1007/s10071-009-0248-6
Hobaiter C, Byrne R (2011a) The gestural repertoire of the wild chimpanzee. Anim Cogn 14:745–767. https://doi.org/10.1007/s10071-011-0409-2
Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cogn 14:827–838
Hobaiter C, Byrne RW (2012) Gesture in consortship: wild chimpanzees’ use of gesture for an ‘evolutionary urgent’ purpose. In: Pika S, Liebal K (eds) Developments in primate gesture research. John Benjamins Publishing Company, Amsterdam, pp 129–146
Hobaiter C, Byrne RW (2014) The meanings of chimpanzee gestures. Curr Biol 24:1596–1600
Hobaiter C, Leavens DA, Byrne RW (2014) Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases. J Comp Psychol 128:82
Hostetter A, Russell J, Freeman H, Hopkins W (2007) Now you see me, now you don’t: evidence that chimpanzees understand the role of the eyes in attention. Anim Cogn 10:55–62. https://doi.org/10.1007/s10071-006-0031-x
Itti L, Koch C (2000) A saliency-based search mechanism for overt and covert shifts of visual attention. Vis Res 40:1489–1506
Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7:216–223. https://doi.org/10.1007/s10071-004-0214-2
Keller H, Lohaus A, Völker S et al (1999) Temporal contingency as an independent component of parenting behavior. Child Dev 70:474–485
Khan RA, Meyer A, Konik H, Bouakaz S (2018) Saliency based framework for facial expression recognition. Front Comput Sci. https://doi.org/10.1007/s11704-017-6114-9
Klein JT, Shepherd SV, Platt ML (2009) Social attention and the brain. Curr Biol 19:R958–R962
Lamaury A, Cochet H, Bourjade M (2017) Acquisition of joint attention by olive baboons gesturing towards humans. Anim Cogn. https://doi.org/10.1007/s10071-017-1111-9
Lavelli M, Fogel A (2013) Interdyad differences in early mother–infant face-to-face communication: real-time dynamics and developmental pathways. Dev Psychol 49:2257
Leavens DA (2004) Manual deixis in apes and humans. Interact Stud 5:387–408. https://doi.org/10.1075/is.5.3.05lea
Leavens DA, Bard KA (2011) Environmental influences on joint attention in great Apes: implications for human cognition. J Cogn Educ Psychol 10:9–31. https://doi.org/10.1891/1945-8959.10.1.9
Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822. https://doi.org/10.1037/0012-1649.34.5.813
Leavens DA, Hopkins WD (1999) The whole-hand point: the structure and function of pointing from a comparative perspective. J Comp Psychol 113:417–425. https://doi.org/10.1037/0735-7036.113.4.417
Leavens DA, Russell JL, Hopkins WD (2005) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76:291–306. https://doi.org/10.1111/j.1467-8624.2005.00845.x
Leavens DA, Bard KA, Hopkins WD (2017) The mismeasure of ape social cognition. Anim Cogn 1–18. https://doi.org/10.1007/s10071-017-1119-1
Liebal K, Call J, Tomasello M (2004) Chimpanzee gesture sequences. Primates 64:377–396
Liebal K, Pika S, Tomasello M (2006) Gestural communication of orangutans (Pongo pygmaeus). Gesture 6:1–38
Liszkowski U, Carpenter M, Henning A et al (2004) Twelve-month-olds point to share attention and interest. Dev Sci 7:297–307
Lucca K, MacLean EL, Hare B (2018) The development and flexibility of gaze alternations in bonobos and chimpanzees. Dev Sci. https://doi.org/10.1111/desc.12598
Lyn H (2017) The question of capacity: why enculturated and trained animals have much to tell Us about the evolution of language. Psychon Bull Rev 24:85–90. https://doi.org/10.3758/s13423-016-1129-z
Lyn H, Russell JL, Leavens DA et al (2014) Apes communicate about absent and displaced objects: methodology matters. Anim Cogn 17:85–94. https://doi.org/10.1007/s10071-013-0640-0
Maille A, Engelhart L, Bourjade M, Blois-Heulin C (2012) To beg, or not to beg? That is the question: mangabeys modify their production of requesting gestures in response to human’s attentional states. PLoS ONE 7:e41197. https://doi.org/10.1371/journal.pone.0041197
Marentette P, Nicoladis E (2012) Does ontogenetic ritualization explain early communicative gestures in human infants? Dev Primate Gesture Res 6:33
Meunier H, Prieur J, Vauclair J (2013) Olive baboons communicate intentionally by pointing. Anim Cogn 16:155–163. https://doi.org/10.1007/s10071-012-0558-y
Mondada L (2014) Instructions in the operating room: how the surgeon directs their assistant’s hands. Discourse Stud 16:131–161
Moore R (2016) Meaning and ostension in great ape gestural communication. Anim Cogn 19:223–231
Murdock BB Jr (1962) The serial position effect of free recall. J Exp Psycho 64(5):482
Newport EL (1975) Motherese: The speech of mothers to young children. ProQuest Information & Learning, Ann Arbor
Parr LA, Winslow JT, Hopkins WD, de Waal F (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:47
Penn DC, Povinelli DJ (2013) The comparative delusion: The “behavioristic/mentalistic” dichotomy in comparative theory of mind and research. In: Metcalfe J, Terrace H (eds) Agency and joint attention. Oxford University Press, New York, pp 62–81
Pika S (2008) Gestures of apes and pre-linguistic human children: similar or different? First Lang 28:116–140. https://doi.org/10.1177/0142723707080966
Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol CB 16:R191–R192. https://doi.org/10.1016/j.cub.2006.02.037
Pika S, Liebal K, Tomasello M (2005) Gestural communication in subadult bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61. https://doi.org/10.1002/ajp.20096
Povinelli DJ, Eddy TJ (1996) Factors influencing young chimpanzees’ (Pan troglodytes) recognition of attention. J Comp Psychol 110:336–345. https://doi.org/10.1037/0735-7036.110.4.336
Reaux JE, Theall LA, Povinelli DJ (1999) A longitudinal investigation of chimpanzees’ understanding of visual perception. Child Dev 70:275–290
Roberts AI, Vick S-J, Buchanan-Smith HM (2013) Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signalling. Anim Cogn 16:187–196
Rochat P, Querido JG, Striano T (1999) Emerging sensitivity to the timing and structure of protoconversation in early infancy. Dev Psychol 35:950
Russell CL, Bard KA, Adamson LB (1997) Social referencing by young chimpanzees (Pan troglodytes). J Comp Psychol 111:185–193. https://doi.org/10.1037/0735-7036.111.2.185
Scott-Phillips TC (2015) Nonhuman primate communication, pragmatics, and the origins of language. Curr Anthropol 56:56–80
Seyfarth RM, Cheney DL (1986) Vocal development in vervet monkeys. Anim Behav 34:1640–1658
Shettleworth SJ (2010) Clever animals and killjoy explanations in comparative psychology. Trends Cogn Sci 14:477–481
Slaughter V, McConnell D (2003) Emergence of joint attention: relationships between gaze following, social referencing, imitation, and naming in infancy. J Genet Psychol 164:54–71
Snowdon CT, Hausberger M (1997) Social influences on vocal development. Cambridge University Press, Cambridge
Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. https://doi.org/10.1007/s00265-010-1037-6
Taylor MJ, Edmonds GE, McCarthy G, Allison T (2001) Eyes first! Eye processing develops before face processing in children. Neuroreport 12:1671–1676
Tempelmann S, Kaminski J, Liebal K (2011) Focus on the essential: all great apes know when others are being attentive. Anim Cogn 14:433–439. https://doi.org/10.1007/s10071-011-0378-5
Tomasello M (1999) Social cognition before the revolution. Early Soc Cogn Underst First Mon Life 301–314
Tomasello M (2014) A natural history of human thinking. Harvard University Press, Harvard
Tomasello M, George BL, Kruger AC et al (1985) The development of gestural communication in young chimpanzees. J Hum Evol 14:175–186. https://doi.org/10.1016/S0047-2484(85)80005-1
Tomasello M, Carpenter M, Liszkowski U (2007) A new look at infant pointing. Child Dev 78:705–722
Townsend SW, Koski SE, Byrne RW et al (2016) Exorcising Grice’s ghost: an empirical approach to studying intentional communication in animals. Biol Rev. https://doi.org/10.1111/brv.12289/full
Wagenmakers E-J, Farrell S (2004) AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196. https://doi.org/10.3758/BF03206482
West MJ, King AP, White DJ (2003) The case for developmental ecology. Anim Behav 66:617–622
Zajonc R (1965) Social Facilitation. Sci N Y Ny 149:269
Zuberbühler K (2008) Audience effects. Curr Biol 18:R189–R190
Acknowledgements
This research was supported by the French National Research Agency (ANR) [Grant number ANR-12-PDOC-0014]. We thank Gaëtan Lagier, Delphine Potdevin and Quentin Wohlfarth for coding all the video material, Morgane Allanic, Brigitte Rimbaud, Valérie Moulin, Yves Gobin and Romain Lacoste for technical support and Luke Glowacki for language editing. We are grateful to Jacques Vauclair, Pauline Fresnais, Stéphane Vautier and Joël Fagot for fruitful discussions over the course of the study.
Funding
This study was funded by the ANR (Grant number ANR-12-PDOC-0014).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Marie Bourjade declares that she has no conflict of interest; Florence Gaunet declares that she has no conflicts of interest; Anaïs Maugard declares that she has no conflict of interest; Adrien Meguerditchian declares that he has no conflict of interest. Adrien Meguerditchian received a grant from the ANR (ANR-12-PDOC-0014).
Ethical approval
All procedures complied with the current French law and the current European directive (reference 86/609/CEE) relative to the protection of animals used for scientific purposes (Station de Primatologie’s agreement number for conducting experiments on vertebrate animals: D13-087-7).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bourjade, M., Gaunet, F., Maugard, A. et al. Manipulating social cues in baboon gesture learning: what does it tell us about the evolution of communication?. Anim Cogn 22, 113–125 (2019). https://doi.org/10.1007/s10071-018-1227-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-018-1227-6