Advertisement

International Journal of Primatology

, Volume 39, Issue 4, pp 602–632 | Cite as

Do Mechanical Effectiveness and Recipient Species Influence Intentional Signal Laterality in Captive Chimpanzees (Pan troglodytes)?

  • Jacques PrieurEmail author
  • Simone Pika
  • Stéphanie Barbu
  • Catherine Blois-Heulin
Article

Abstract

Studying the relationships between the directions of brain lateralization for handedness and language can shed light on mechanisms underlying hemispheric specialization for manipulation and signalling functions. We investigated the influence of manipulation and communication functions and of recipient species (conspecific- versus human-directed communication) on manual laterality in signalling context, taking several factors into account simultaneously. We assessed laterality in 39 chimpanzees (Pan troglodytes), including 4 manipulators (mechanically effective social actions used to get things done) and 18 gestures (mechanically ineffective social actions implying that the signaller takes the recipient’s response into account). We focused on the following factors: interactional context components (e.g., visual fields of both interactants), degree of use of signals (“rare” for signals performed by only a few subjects in the population or “common” for signals performed by many subjects), mechanical effectiveness, subjects’ sociodemographic characteristics (e.g., age and hierarchy), and recipient species. We found a significant population-level right-hand bias for one type of human-directed gesture (slap hand). Mechanical effectiveness influenced laterality: right-hand use was more pronounced for conspecific-directed gestures than for conspecific-directed manipulators. The laterality of conspecific-directed gestures overall did not differ from that of human-directed gestures. However, we found an indirect influence of recipient species on laterality as conspecific- and human-directed gestural lateralities were modulated differently by the position of the recipient in the signaller’s visual field and by signaller’s age. We hypothesize that the communication nature of gestures might have developed from manipulators. Manipulators may have contributed to the emergence and the evolution of the left-lateralized communication system in primates.

Keywords

Gestural communication Hemispheric lateralization Language evolution Manipulation Motor effectiveness Primate lateral asymmetry 

Notes

Acknowledgments

We are very grateful to all the keepers, collaborators, and researchers of the Wolfgang Köhler Primate Research Center at Zoo Leipzig, Germany; the Zooparc de Beauval; and the zoo of La Palmyre, France; and particularly Daniel Hanus, Josep Call, Aude Desmoulins, Romain Potier, Florence Perroux, and Thierry Petit for allowing us to study their chimpanzee groups as well as for their friendliness and helpfulness. We are also indebted to Amandine Chapelain for her advice about the design of the observation protocol and to Russell Lenth and Maxime Hervé for their statistical advice about the use of lme4 and lsmeans packages as well as to Ann Cloarec for correcting the English. Furthermore, we thank the editor and reviewers for helpful comments on this article. This study has been performed in the framework of a PhD funded by the French Ministry of Research and Technology with additional financial support of Rennes Metropole and the VAS Doctoral School. In addition, it was supported by a Sofja-Kovalevskaja Award of the Humboldt Foundation to S. Pika.

Supplementary material

10764_2018_54_MOESM1_ESM.pdf (465 kb)
ESM 1 (PDF 465 kb)

References

  1. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arbib, M. A., Liebal, K., & Pika, S. (2008). Primate vocalization, gesture, and the evolution of human language. Current Anthropology, 49(6), 1053–1063.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Badzakova-Trajkov, G., Häberling, I. S., Roberts, R. P., & Corballis, M. C. (2010). Cerebral asymmetries: complementary and independent processes. PloS one, 5(3), e9682.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baraud, I., Buytet, B., Bec, P., & Blois-Heulin, C. (2009). Social laterality and ‘transversality’ in two species of mangabeys: Influence of rank and implication for hemispheric specialization. Behavioural Brain Research, 198(2), 449–458.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bates, E., Benigni, L., Bretherton, I., Camaioni, L., & Volterra, V. (1979). The emergence of symbols: Communication and cognition in infancy. New York: Academic Press.Google Scholar
  6. Bates, E., O’Connell, B., Vaid, J., Sledge, P., & Oakes, L. (1986). Language and hand preference in early development. Developmental Neuropsychology, 2, 1–15.CrossRefGoogle Scholar
  7. Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). _lme4: Linear mixed-effects models using Eigen and S4_. R package version 1.1–7, http://CRAN.R-project.org/package=lme4.
  8. Bruner, J. S. (1981). Intention in the structure of action and interaction. In L. P. Lipsitt (Ed.), Advances in infancy research (Vol. 1, pp. 41–56). Norwood: Ablex.Google Scholar
  9. Byrne, R. W., & Byrne, J. M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. berengei). Cortex, 27, 521–546.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Call, J., & Tomasello, M. (2007). The gestural communication of apes and monkeys. Mahwah: Psychology Press.Google Scholar
  11. Cicchetti, D. V., & Feinstein, A. R. (1990). High agreement but low kappa: II. Resolving the paradoxes. Journal of clinical epidemiology, 43(6), 551–558.CrossRefPubMedGoogle Scholar
  12. Cochet, H., & Vauclair, J. (2012). Hand preferences in human adults: Non-communicative actions versus communicative gestures. Cortex, 48(8), 1017–1026.CrossRefPubMedGoogle Scholar
  13. Cochet, H., Jover, M., & Vauclair, J. (2011). Hand preference for pointing gestures and bimanual manipulation around the vocabulary spurt period. Journal of Experimental Child Psychology, 110(3), 393–407.CrossRefPubMedGoogle Scholar
  14. Corballis, M. C. (2002). From hand to mouth: The origins of language. Princeton: Princeton University Press.Google Scholar
  15. Crockford, C., & Boesch, C. (2005). Call combinations in wild chimpanzees. Behaviour, 142, 397–421.CrossRefGoogle Scholar
  16. Damerose, E., & Vauclair, J. (2002). Posture and laterality in human and non-human primates: asymmetries in maternal handling and the infant’s early motor asymmetries. Comparative vertebrate lateralization, 306–362.Google Scholar
  17. de Vries, H. (1995). An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Animal Behaviour, 50, 1375–1389.CrossRefGoogle Scholar
  18. de Vries, H. (1998). Finding a dominance order most consistent with a linear hierarchy: A new procedure and review. Animal Behaviour, 55, 827–843.CrossRefPubMedGoogle Scholar
  19. de Vries, H., Stevens, J. M. G., & Vervaecke, H. (2006). Measuring and testing the steepness of dominance hierarchies. Animal Behaviour, 71, 585–592.CrossRefGoogle Scholar
  20. de Waal, F. B. (1988). The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour, 106(3), 183–251.CrossRefGoogle Scholar
  21. Elliott, J. M., & Connolly, K. J. (1984). A classification of manipulative hand movements. Developmental Medicine & Child Neurology, 26(3), 283–296.CrossRefGoogle Scholar
  22. Fabbri-Destro, M., & Rizzolatti, G. (2008). Mirror neurons and mirror systems in monkeys and humans. American Physiological Society, Physiology, 23(3), 171–179.Google Scholar
  23. Fagard, J. (2013). The nature and nurture of human infant hand preference. Annals of the New York Academy of Sciences, 1288(1), 114–123.CrossRefPubMedGoogle Scholar
  24. Fedigan, L. M. (2010). Ethical issues faced by field primatologists: Asking the relevant questions. American Journal of Primatology, 72(9), 754–771.CrossRefPubMedGoogle Scholar
  25. Feinstein, A. R., & Cicchetti, D. V. (1990). High agreement but low kappa: I. The problems of two paradoxes. Journal of clinical epidemiology, 43(6), 543–549.CrossRefPubMedGoogle Scholar
  26. Forrester, G. S., Quaresmini, C., Leavens, D. A., Spiezio, C., & Vallortigara, G. (2012). Target animacy influences chimpanzee handedness. Animal cognition, 15(6), 1121–1127.CrossRefPubMedGoogle Scholar
  27. Forrester, G. S., Quaresmini, C., Leavens, D. A., Mareschal, D., & Thomas, M. S. (2013). Human handedness: An inherited evolutionary trait. Behavioural Brain Research, 237, 200–206.CrossRefPubMedGoogle Scholar
  28. Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology, 65(1), 47–55.CrossRefPubMedGoogle Scholar
  29. Fox, J., & Weisberg, S. (2011). An R companion to applied regression (2nd ed.). Thousand Oaks: SAGE.Google Scholar
  30. Fröhlich, M., Kuchenbuch, P., Müller, G., Fruth, B., Furuichi, T., et al (2016). Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. Scientific Reports, 6. 25887.  https://doi.org/10.1038/srep25887.
  31. Gentilucci, M., & Corballis, M. C. (2006). From manual gesture to speech: A gradual transition. Neuroscience & Biobehavioral Reviews, 30(7), 949–960.CrossRefGoogle Scholar
  32. Ghirlanda, S., & Vallortigara, G. (2004). The evolution of brain lateralization: a game-theoretical analysis of population structure. Proceedings of the Royal Society B: Biological Sciences, 271(1541), 853.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ghirlanda, S., Frasnelli, E., & Vallortigara, G. (2009). Intraspecific competition and coordination in the evolution of lateralization. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1519), 861–866.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Goodall, J. (1986). The chimpanzees of Gombe: Patterns in adaptation. Cambridge: Harvard University Press.Google Scholar
  35. Häberling, I. S., Corballis, P. M., & Corballis, M. C. (2016). Language, gesture, and handedness: Evidence for independent lateralized networks. Cortex, 82, 72–85.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Harris, L. J., & Carlson, D. F. (1993). Hand preference for visually-guided reaching in human infants and adults. In J. P. Ward & W. D. Hopkins (Eds.), Primate laterality: Current behavioural evidence of primate asymmetries (pp. 285–305). New York: Springer-Verlag.CrossRefGoogle Scholar
  37. Harrison, R. M., & Nystrom, P. (2010). Handedness in captive gorillas (Gorilla gorilla). Primates, 51, 251–261.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hervé, M. (2014). RVAideMemoire: Diverse basic statistical and graphical functions. R package version 0.9–40. http://CRAN.R-project.org/package=RVAideMemoire.
  39. Hopkins, W. D. (2004). Laterality in maternal cradling and infant positional biases: Implications for the development and evolution of hand preferences in nonhuman primates. International Journal of Primatology, 25(6), 1243–1265.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hopkins, W. D., & de Waal, F. B. (1995). Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension. International Journal of Primatology, 16(3), 261–276.CrossRefGoogle Scholar
  41. Hopkins, W. D., & Leavens, D. A. (1998). Hand use and gestural communication in chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 112(1), 95–99.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hopkins, W. D., Russell, J., Freeman, H., Buehler, N., Reynolds, E., & Schapiro, S. J. (2005a). The distribution and development of handedness for manual gestures in captive chimpanzees (Pan troglodytes). Psychological Science, 16(6), 487–493.PubMedPubMedCentralGoogle Scholar
  43. Hopkins, W. D., Russell, J. L., Cantalupo, C., Freeman, H., & Schapiro, S. J. (2005b). Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 119(4), 363–370.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hopkins, W. D., Pika, S., Liebal, K., Bania, A., Meguerditchian, A., et al (2012). Handedness for manual gestures in great apes: A meta-analysis. In S. Pika & K. Liebal (Eds.), Developments in primate gesture research (pp. 93–110). Amsterdam: John Benjamins.CrossRefGoogle Scholar
  45. Hostetter, A. B., Cantero, M., & Hopkins, W. D. (2001). Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). Journal of Comparative Psychology, 115(4), 337.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jacquet, A. Y., Esseily, R., Rider, D., & Fagard, J. (2012). Handedness for grasping objects and declarative pointing: a longitudinal study. Developmental Psychobiology, 54(1), 36–46.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kano, T. (1992). The last ape: Pygmy chimpanzee behavior and ecology. Stanford: Stanford University Press.Google Scholar
  48. Kano, T. (1998). A preliminary glossary of bonobo behaviors at Wamba. In T. Nishida (Ed.), Comparative study of the behavior of the genus Pan by compiling video ethogram (pp. 39–81). Kyoto: Nissho Printer.Google Scholar
  49. Kimura, D. (1973). Manual activity during speaking— I. Right-handers. Neuropsychologia, 11(1), 45–50.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Knecht, S., Dräger, B., Deppe, M., Bobe, L., Lohmann, H., Flöel, A., et al. (2000). Handedness and hemispheric language dominance in healthy humans. Brain, 123(12), 2512–2518.CrossRefPubMedGoogle Scholar
  51. Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data. biometrics, 159-174.Google Scholar
  52. Langbein, J., & Puppe, B. (2004). Analysing dominance relationships by sociometric methods—a plea for a more standardised and precise approach in farm animals. Applied Animal Behaviour Science, 87, 293–315.CrossRefGoogle Scholar
  53. Leavens, D. A., & Hopkins, W. D. (1998). Intentional communication by chimpanzees: A cross-sectional study of the use of referential gestures. Developmental Psychology, 34(5), 813.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Leavens, D. A., Reamer, L. A., Mareno, M. C., Russell, J. L., Wilson, D., et al (2015). Distal communication by chimpanzees (Pan troglodytes): Evidence for common ground? Child Development, 86(5), 1623–1638.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lenth, R. V. (2014). lsmeans: Least-squares means. R package version 2.11. http://CRAN.R-project.org/package=lsmeans.
  56. Liebal, K., & Call, J. (2012). The origins of non-human primates’ manual gestures. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 118–128.CrossRefGoogle Scholar
  57. Liebal, K., Call, J., & Tomasello, M. (2004). Use of gesture sequences in chimpanzees. American Journal of Primatology, 64(4), 377–396.CrossRefPubMedGoogle Scholar
  58. Liu, H., Stufflebeam, S. M., Sepulcre, J., Hedden, T., & Buckner, R. L. (2009). Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors. Proceedings of the National Academy of Sciences.Google Scholar
  59. Llaurens, V., Raymond, M., & Faurie, C. (2009). Why are some people left-handed? An evolutionary perspective. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1519), 881–894.CrossRefPubMedGoogle Scholar
  60. Maille, A., Chapelain, A., Déruti, L., Bec, P., & Blois-Heulin, C. (2013). Manual laterality for pointing gestures compared to grasping actions in guenons and mangabeys. Animal Behaviour, 86(4), 705–716.CrossRefGoogle Scholar
  61. Manning, J. T., & Chamberlain, A. T. (1991). Left-side cradling and brain lateralization. Ethology and Sociobiology, 12(3), 237–244.CrossRefGoogle Scholar
  62. Marchant, L. F., & McGrew, W. C. (1991). Laterality of function in apes: A meta-analysis of methods. Journal of Human Evolution, 21, 425–438.CrossRefGoogle Scholar
  63. Marchant, L. F., & McGrew, W. C. (2013). Handedness is more than laterality: Lessons from chimpanzees. Annals of the New York Academy of Sciences, 1288(1), 1–8.CrossRefPubMedGoogle Scholar
  64. Martin, P., & Bateson, P. (1994). Measuring behaviour: An introductory guide (2nd ed.). Cambridge: Cambridge University Press.Google Scholar
  65. Mazoyer, B., Zago, L., Jobard, G., Crivello, F., Joliot, M., Perchey, G., et al. (2014). Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PloS one, 9(6), e101165.CrossRefPubMedPubMedCentralGoogle Scholar
  66. McGrew, W. C., & Marchant, L. F. (1997). On the other hand: Current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearbook of Physical Anthropology, 40, 201–232.CrossRefGoogle Scholar
  67. McManus, I. C. (1991). The inheritance of left-handedness. In Biological asymmetry and handedness (Ciba Foundation Symposium), 162, 251–281. Chichester: John Wiley & Sons.Google Scholar
  68. McManus, I. C., Davison, A., & Armour, J. A. (2013). Multilocus genetic models of handedness closely resemble single-locus models in explaining family data and are compatible with genome-wide association studies. Annals of the New York Academy of Sciences, 1288(1), 48–58.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Meguerditchian, A., & Vauclair, J. (2006). Baboons communicate with their right hand. Behavioural Brain Research, 171(1), 170–174.CrossRefPubMedGoogle Scholar
  70. Meguerditchian, A., & Vauclair, J. (2009). Contrast of hand preferences between communicative gestures and non-communicative actions in baboons: Implications for the origins of hemispheric specialization for language. Brain and Language, 108(3), 167.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Meguerditchian, A., & Vauclair, J. (2014). Communicative signaling, lateralization and brain substrate in nonhuman primates: Toward a gestural or a multimodal origin of language? Humana. Mente Journal of Philosophical Studies, 27, 135–160.Google Scholar
  72. Meguerditchian, A., Vauclair, J., & Hopkins, W. D. (2010). Captive chimpanzees use their right hand to communicate with each other: Implications for the origin of the cerebral substrate for language. Cortex, 46(1), 40–48.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Meguerditchian, A., Molesti, S., & Vauclair, J. (2011). Right-handedness predominance in 162 baboons (Papio anubis) for gestural communication: Consistency across time and groups. Behavioral Neuroscience, 125(4), 653–660.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Meguerditchian, A., Vauclair, J., & Hopkins, W. D. (2013). On the origins of human handedness and language: A comparative review of hand preferences for bimanual coordinated actions and gestural communication in nonhuman primates. Developmental Psychobiology, 55, 637–650.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Nishida, T., Kano, T., Goodall, J., McGrew, W. C., & Nakamura, M. (1999). Ethogram and ethnography of Mahale chimpanzees. Anthropological Science, 107, 141–188.CrossRefGoogle Scholar
  76. Ocklenburg, S., Beste, C., & Güntürkün, O. (2013). Handedness: A neurogenetic shift of perspective. Neuroscience & Biobehavioral Reviews, 37(10), 2788–2793.CrossRefGoogle Scholar
  77. Ocklenburg, S., Beste, C., Arning, L., Peterburs, J., & Güntürkün, O. (2014). The ontogenesis of language lateralization and its relation to handedness. Neuroscience & Biobehavioral Reviews, 43, 191–198.CrossRefGoogle Scholar
  78. Palmer, A. R. (2002). Chimpanzee right-handedness reconsidered: Evaluating the evidence with funnel plots. American Journal of Physical Anthropology, 118(2), 191–199.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Parr, L. A., & Waller, B. M. (2006). Understanding chimpanzee facial expression: insights into the evolution of communication. Social Cognitive and Affective Neuroscience, 1(3), 221–228.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Pika, S. (2008). What is the nature of the gestural communication of great apes. In J. Zlatev, T. Racine, C. Sinha, & E. Itkonen (Eds.), The shared mind: Perspectives on intersubjectivity (pp. 165–186). Amsterdam: John Benjamins.CrossRefGoogle Scholar
  81. Pika, S., & Bugnyar, T. (2011). The use of referential gestures in ravens (Corvus corax) in the wild. Nature Communications, 2, 560.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Pika, S., & Fröhlich, M. (2018). Gestural acquisition in great apes: The Social Negotiation Hypothesis. Animal Cognition.  https://doi.org/10.1007/s10071-017-1159-6.
  83. Pika, S., & Mitani, J. C. (2006). Referential gesturing in wild chimpanzees (Pan troglodytes). Current Biology, 16, 191–192.CrossRefGoogle Scholar
  84. Pika, S., Liebal, K., & Tomasello, M. (2003). Gestural communication in young gorillas (Gorilla gorilla): Gestural repertoire, learning, and use. American Journal of Primatology, 60, 95–111.CrossRefPubMedGoogle Scholar
  85. Pika, S., Liebal, K., & Tomasello, M. (2005a). Gestural communication in subadult bonobos (Pan paniscus): Repertoire and use. American Journal of Primatology, 65, 39–61.CrossRefPubMedGoogle Scholar
  86. Pika, S., Liebal, K., Call, J., & Tomasello, M. (2005b). Gestural communication of apes. Gesture, 5(1), 41–56.CrossRefGoogle Scholar
  87. Pollick, A. S., & de Waal, F. (2007). Ape gestures and language evolution. Proceedings of the National Academy of Sciences of the USA, 104, 8184–8189.CrossRefPubMedGoogle Scholar
  88. Prieur, J. (2015). Chimpanzees' and gorillas' intraspecific gestural laterality: A multifactorial investigation. Doctorate thesis, Rennes, France: University of Rennes 1. www.theses.fr/en/2015REN1S056.
  89. Prieur, J., Pika, S., Barbu, S., & Blois-Heulin, C. (2016a). A multifactorial investigation of captive chimpanzees’ intraspecific gestural laterality. Animal Behaviour, 116, 31–43.CrossRefGoogle Scholar
  90. Prieur, J., Pika, S., Barbu, S., & Blois-Heulin, C. (2016b). Gorillas are right-handed for their most frequent intraspecific gestures. Animal Behaviour, 118, 165–170.CrossRefGoogle Scholar
  91. Prieur, J., Lemasson, A., Barbu, S., & Blois-Heulin, C. (2018a). Challenges facing the study of the evolutionary origins of human right-handedness and language. International Journal of Primatology, 38(2), 183–207.CrossRefGoogle Scholar
  92. Prieur, J., Barbu, S., & Blois-Heulin, C. (2018b). Human laterality for manipulation and gestural communication related to 60 everyday activities: Impact of multiple individual-related factors. Cortex, 99, 118–134.CrossRefPubMedGoogle Scholar
  93. Prieur J., Le Du G., Stomp M., Barbu S., & Blois-Heulin C. (unpubl. data). Human laterality for manipulation and gestures: A study of beach-volleyball players during the 2012 Olympic Games. Google Scholar
  94. R Development Core Team (2014). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing http://www.R-project.org.Google Scholar
  95. Rohlfs, P., & Ramirez, J. M. (2006). Aggression and brain asymmetries: A theoretical overview. Aggression and Violent Behavior, 11, 283–297.CrossRefGoogle Scholar
  96. Roth, R. R. (1995). A study of gestural communication during sexual behavior in bonobo (Pan paniscus, Schwartz) (pp. 1–119). Calgary: University of Calgary Press.Google Scholar
  97. Schaafsma, S. M., Riedstra, B. J., Pfannkuche, K. A., Bouma, A., & Groothuis, T. G. G. (2009). Epigenesis of behavioural lateralization in humans and other animals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1519), 915–927.CrossRefPubMedGoogle Scholar
  98. Scott, N. M., & Pika, S. (2012). A call for conformity. Developments in Primate Gesture Research, 6, 147.CrossRefGoogle Scholar
  99. Taglialatela, J. P., Russell, J. L., Pope, S. M., Morton, T., Bogart, S., et al (2015). Multimodal communication in chimpanzees. American Journal of Primatology, 77(11), 1143–1148.CrossRefPubMedPubMedCentralGoogle Scholar
  100. Tzourio-Mazoyer, N., Petit, L., Zago, L., Crivello, F., Vinuesa, N., Joliot, M., et al. (2015). Between-hand difference in ipsilateral deactivation is associated with hand lateralization: fMRI mapping of 284 volunteers balanced for handedness. Frontiers in Human Neuroscience, 9, 5.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Vallortigara, G., & Rogers, L. J. (2005). Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behavioral and brain sciences, 28(4), 575–588.PubMedGoogle Scholar
  102. Van Hooff, J. A. R. A. M. (1973). A structural analysis of the social behaviour of a semi-captive group of chimpanzees. Social Communication and Movement: Studies of Interaction and Expression in Man and Chimpanzee (pp. 75–162). European Monographs in Social Psychology, 4. London: Academic Press.Google Scholar
  103. Vauclair, J., & Imbault, J. (2009). Relationship between manual preferences for object manipulation and pointing gestures in infants and toddlers. Developmental Science, 12(6), 1060–1069.CrossRefPubMedGoogle Scholar
  104. Versace, E., & Vallortigara, G. (2015). Forelimb preferences in human beings and other species: multiple models for testing hypotheses on lateralization. Frontiers in Psychology, 6, 233.Google Scholar
  105. Waller, B. M., Warmelink, L., Liebal, K., Micheletta, J., & Slocombe, K. E. (2013). Pseudoreplication: A widespread problem in primate communication research. Animal Behaviour, 86(2), 483–488.CrossRefGoogle Scholar
  106. Wallez, C., Schaeffer, J., Meguerditchian, A., Vauclair, J., Schapiro, S. J., & Hopkins, W. D. (2012). Contrast of hemispheric lateralization for oro-facial movements between learned attention-getting sounds and species-typical vocalizations in chimpanzees: Extension in a second colony. Brain and Language, 123(1), 75–79.CrossRefPubMedGoogle Scholar
  107. Yen, K., Kuppermann, N., Lillis, K., Monroe, D., Borgialli, D., Kerrey, B. T., et al. (2013). Interobserver agreement in the clinical assessment of children with blunt abdominal trauma. Academic Emergency Medicine, 20(5), 426–432.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jacques Prieur
    • 1
    Email author
  • Simone Pika
    • 2
    • 3
  • Stéphanie Barbu
    • 1
  • Catherine Blois-Heulin
    • 1
  1. 1.Université de Rennes, Ethologie Animale et Humaine, UMR 6552, CNRS, Université de Caen NormandiePaimpontFrance
  2. 2.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  3. 3.Comparative Biocognition, Institute of Cognitive ScienceUniversity of OsnabrückOsnabrückGermany

Personalised recommendations