, Volume 60, Issue 6, pp 507–515 | Cite as

Social relationships and greetings in wild chimpanzees (Pan troglodytes): use of signal combinations

  • Eva Maria LuefEmail author
  • Simone Pika
Original Article


Signals of submission, so-called ‘greetings’, represent an important tool for the regulation of social life in primates. In chimpanzees, vocalizations and gestures are commonly employed to communicate greetings, however, the topic of signal complexity (i.e., combinations of signals) during greeting instances has been neglected by research to date. Here, we investigate combinatorial possibilities in vocal greetings in a free-ranging group of chimpanzees (Pan troglodytes) and study how greeter sex, rank relationship between an interacting pair, and strength of the social bond of a greeting dyad influence signal complexity. Results show that the social bond and the dominance distance between individuals engaged in a greeting bout are important determiners for vocal combinations. The findings indicate that greeting signals in chimpanzees, like other vocal signals of the species, can become subject to social influences.


Chimpanzees Pan troglodytes Ngogo Greeting Pant-grunt Combinations Repetitions 



This paper is dedicated to the memory of J. Lwanga. We are indebted to J. C. Mitani, D. Watts and K. Langergraber for the opportunity to carry out research at Ngogo. Without their continuous support this work would not have been possible. We thank the Makerere University Biological Field Station (MUBFS; Uganda), the Uganda National Council for Science and Technology (UNCST; Uganda) and the Uganda Wildlife Authority (UWA; Uganda) for granting permission to conduct research at Kibale National Park. We are indebted to the whole staff at Ngogo, particularly D. Kyalikunda, for assisting us and sharing their deep knowledge on the chimpanzee community and the forest. We furthermore thank A. ter Maat for assisting with the acoustical analyses, C. Neumann for his R-script on Elo-ranking, and R. Mundry for his invaluable statistical help with the models. This research was funded by a Sofja-Kovalevskaja-Award of the Alexander-von-Humboldt Foundation (Germany) to S. P. The work described in this manuscript has complied with the ethical standards in the treatment of animals with the guidelines laid down by the Primate Society of Japan, NIH (US), EC Guide for animal experiments, and the legal requirements concerning animal treatment and welfare in Uganda and Germany. The authors declare that they have no conflicts of interest.

Supplementary material

10329_2019_758_MOESM1_ESM.pdf (6.9 mb)
Supplementary material 1 (PDF 7114 kb)
10329_2019_758_MOESM2_ESM.pdf (243 kb)
Supplementary material 2 (PDF 243 kb)


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behavior 49:227–266Google Scholar
  2. Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, CambridgeGoogle Scholar
  3. Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278Google Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2014) {lme4}: Linear mixed-effects models using Eigen and S4. R Package version 11–7Google Scholar
  5. Beecher MD, Campbell SE, Burt JM, Hill CE, Nordby JC (2000) Song-type matching between neighbouring song sparrows. Anim Behav 59:21–27PubMedGoogle Scholar
  6. Bergman TJ, Sheehan MJ (2013) Social knowledge and signals in primates. Am J Primatol 75:683–694PubMedGoogle Scholar
  7. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer, SunderlandGoogle Scholar
  8. Bygott JD (1979) Agonistic behavior, dominance, and social structure in wild chimpanzees of Gombe National Park. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Melo Park, pp 405–428Google Scholar
  9. Candiotti A, Zuberbuehler K, Lemasson A (2012) Convergence and divergence in Diana monkey vocalizations. Biol Lett 8:382–385PubMedPubMedCentralGoogle Scholar
  10. Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–364Google Scholar
  11. Cheney DL, Seyfarth RM (1990) How monkeys see the world. University of Chicago Press, ChicagoGoogle Scholar
  12. Clark AP (1993) Rank differences in the production of vocalizations by wild chimpanzees as a function of social context. Am J Primatol 31:159–179Google Scholar
  13. Clutton-Brock TH, Harvey PH (1977) Primate ecology and social organization. J Zool 183:1–39Google Scholar
  14. Crockford C, Boesch C (2003) Context-specific calls in wild chimpanzees, Pan troglodytes verus: analysis of barks. Anim Behav 66:115–125Google Scholar
  15. Crockford C, Boesch C (2005) Call combinations in wild chimpanzees. Behaviour 142:397–421Google Scholar
  16. Crockford C, Wittig RM, Zuberbuehler K (2017) Vocalizing in chimpanzees is influenced by social-cognitive processes. Sci Adv 3:e1701742PubMedPubMedCentralGoogle Scholar
  17. de Waal FB (1982) Chimpanzee politics: Power and sex among apes. Harper & Row, New YorkGoogle Scholar
  18. Dobson AJ (2002) An introduction to generalized linear models. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  19. Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131Google Scholar
  20. East ML, Hofer H, Wickler W (1993) The erect ‘penis’ is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav Ecol Sociobiol 33:355–370Google Scholar
  21. Fallon BL, Neumann C, Byrne RW, Zuberbuehler K (2016) Female chimpanzees adjust copulation calls according to reproductive status and level of female competition. Anim Behav 113:87–92Google Scholar
  22. Fedurek P, Machanda ZP, Schel AM, Slocombe KE (2013) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196Google Scholar
  23. Fedurek P, Neumann C, Bouquet Y, Mercier S, Magris M, Quintero F et al (2019) Behavioural patterns of vocal greeting production in four primate species. Roy Soc Open Sci 6:182181Google Scholar
  24. Field A (2005) Discovering statistics using SPSS. Sage Publications, LondonGoogle Scholar
  25. Fischer J (2013) Information, inference and meaning in primate vocal communication. In: Stegmann U (ed) Animal communication theory: information and influence. Cambridge University Press, Cambridge, pp 297–319Google Scholar
  26. Flack JC, Jeannotte LA, de Waal FB (2004) Play signaling and the perception of social rules by juvenile chimpanzees (Pan troglodytes). J Comp Psychol 118:149–159PubMedGoogle Scholar
  27. Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55PubMedGoogle Scholar
  28. Fox J, Monette G (1992) Generalized collinearity diagnostics. J Am Stat Assoc 87:178–183Google Scholar
  29. Giles H (2016) Communication accommodation theory: negotiating personal relationships and social identities across contexts. Cambridge University Press, CambridgeGoogle Scholar
  30. Goodall J (1986) The chimpanzees of Gombe. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  31. Gwinner E (1964) Untersuchungen über das Ausdrucks- und Sozialverhalten des Kolkraben (Corvus corax). Z Tierpsychol 21:145–178Google Scholar
  32. Hartigan JA (1975) Clustering algorithms. Wiley, HobokenGoogle Scholar
  33. Hayaki H (1990) Social context of pant-grunting in young chimpanzees. In: Nishida T (ed) The chimpanzees of the Mahale mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 189–206Google Scholar
  34. Hohmann G, Fruth B (1995) Loud calls in great apes: sex differences and social correlates. In: Zimmermann E, Newman JD, Juergens U (eds) Current topics in primate vocal communication. Springer, Heidelberg, pp 161–184Google Scholar
  35. Kappeler PM, Van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740Google Scholar
  36. Krebs JR, Dawkins R (1984) Animal signals: mind reading and manipulation. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific Publications, Oxford, pp 380–402Google Scholar
  37. Langergraber KE, Mitani JC, Watts DP, Vigilant L (2013) Male–female socio-spatial relationships and reproduction in wild chimpanzees. Behav Ecol Sociobiol 67:861–873Google Scholar
  38. Laporte MN, Zuberbuehler K (2010) Vocal greeting behaviour in wild chimpanzee females. Anim Behav 80:467–473Google Scholar
  39. Laporte NM, Zuberbuehler K (2011) The development of greeting signals in wild chimpanzees. Dev Sci 14:1220–1234PubMedGoogle Scholar
  40. Lehner PN (2002) Handbook of ethological methods, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  41. Luef EM, Pika S (2016) Reciprocal greeting in chimpanzees (Pan troglodytes) at the Ngogo community. J Neurolinguistics 43:263–273Google Scholar
  42. Luef EM, ter Maat A, Pika S (2017) Vocal similarity in long-distance and short-distance vocalizations in raven pairs (Corvus corax) in captivity. Behav Process 142:1–7Google Scholar
  43. Lwanga JS (2003) Forest succession in Kibale National Park, Uganda: implications for forest restoration and management. Afr J Ecol 41:9–22Google Scholar
  44. Marler P, Tenaza RR (1977) Signaling behavior of apes with special reference to vocalization. In: Sebeok TA (ed) How animals communicate. Indiana University Press, London, pp 965–1033Google Scholar
  45. Marshall AJ, Wrangham RW, Arcadi AC (1999) Does learning affect the structure of vocalizations in chimpanzees? Anim Behav 58:825–830PubMedGoogle Scholar
  46. McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1:381–385PubMedPubMedCentralGoogle Scholar
  47. McCullagh P, Nelder JA (1996) Generalized linear models. Chapman & Hall, LondonGoogle Scholar
  48. Mitani JC (2009) Male chimpanzees form enduring and equitable social bonds. Anim Behav 77:633–640Google Scholar
  49. Mitani JC, Brandt KL (1994) Social factors influence the acoustic variability in the long-distance calls of male chimpanzees. Ethology 96:233–252Google Scholar
  50. Moravec ML, Striedtler GF, Burley NT (2006) Assortative pairing based on contact call similarity in budgerigars, Melopsittacus undulatus. Ethology 112:1108–1116Google Scholar
  51. Moss C, Poole J (1983) Relationships and social structure of African elephants. In: Hinde RA (ed) Primate social relationships: an integrated approach. Sinauer, Sunderland, pp 315–325Google Scholar
  52. Neumann C, Doboscq J, Dubuc C, Ginting A, Irwan AM, Agil M et al (2011) Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour 82:911–921Google Scholar
  53. Nishida T (1968) The social group of wild chimpanzees in the Mahali mountains. Primates 9:167–224Google Scholar
  54. Nishida T (1970) Social behavior and relationship among wild chimpanzees of the Mahali Mountains. Primates 11:47–68Google Scholar
  55. Okamoto K, Agetsuma N, Kojima S (2001) Greeting behavior during party encounters in captive chimpanzees. Primates 42:161–165Google Scholar
  56. Palomares NA, Giles H, Soliz J, Gallois C (2016) Intergroup accommodation, social categories, and identities. In: Giles H (ed) Communication accommodation theory: negotiating personal relationships and social identities across contexts. Cambridge University Press, Cambridge, pp 123–151Google Scholar
  57. Pika S (2017) Unpeeling the layers of communicative complexity. Anim Behav 143:223–227Google Scholar
  58. Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16:R191–R192PubMedGoogle Scholar
  59. Quinn GP, Keough MJ (2002) Experimental designs and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  60. R Developmental Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  61. Roberts SGB, Roberts AI (2016) Social brain hypothesis: vocal and gesture networks of wild chimpanzees. Front Psychol 7:1756PubMedPubMedCentralGoogle Scholar
  62. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420PubMedGoogle Scholar
  63. Silk JB (2007) Social components of fitness in primate groups. Science 317:1347–1351PubMedGoogle Scholar
  64. Silk JB (2014) Evolutionary perspectives on the links between close social bonds, health, and fitness. In: Weinstein M, Lane MA (eds) Sociality, hierarchy, health: comparative biodemography. National Academies Press, Washington, pp 121–144 (A collection of papers) Google Scholar
  65. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1331–1334Google Scholar
  66. Silk JB, Cheney DL, Seyfarth RM (2013) A practical guide to the study of social relationships. Evol Anthropol 22:213–225PubMedGoogle Scholar
  67. Slocombe KE, Zuberbuhler K (2005) Agonistic screams in wild chimpanzees (Pan troglodytes schweinfurthii) vary as a function of social role. J Comp Psychol 119:67–77PubMedGoogle Scholar
  68. Slocombe KE, Kaller T, Turman L, Townsend SW, Papworth S, Squibbs P et al (2010) Production of food-associated calls in wild male chimpanzees is dependent on the composition of the audience. Behav Ecol Sociobiol 64:1959–1966Google Scholar
  69. Snowdon CT (2009) Plasticity of communication in nonhuman primates. Adv Stud Behav 40:239–276Google Scholar
  70. Snowdon CT, Brown CH, Petersen MR (1982) Primate communication. Cambridge University Press, CambridgeGoogle Scholar
  71. Struhsaker TT (1997) Ecology of an African rainforest. University Press of Florida, GainesvilleGoogle Scholar
  72. Taglialatela JP, Russell JL, Pope SM, Morton T, Bogart S, Reamer LA et al (2015) Multimodal communication in chimpanzees. Am J Primatol 77:1143–1148PubMedPubMedCentralGoogle Scholar
  73. ter Maat A, Trost L, Sagunsky H, Seltmann S, Gahr M (2014) Zebra finch mates use their forebrain song system in unlearned call communication. PLoS One 9:e109334PubMedPubMedCentralGoogle Scholar
  74. Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New YorkGoogle Scholar
  75. Tomasello M, Call J, Warren J, Frost GT, Carpenter M, Nagell K (1997) The ontogeny of chimpanzee gestural signals: a comparison across groups and generations. Evol Commun 1:223–259Google Scholar
  76. Watson SK, Townsend S, Schel AM, Wilke C, Wallace EK, Cheng L et al (2015) Vocal learning in the functionally referential food grunts of chimpanzees. Curr Biol 25:495–499PubMedGoogle Scholar
  77. Whiten A (2005) The second inheritance system of chimpanzees and humans. Nature 437:52–55PubMedGoogle Scholar
  78. Whitham JC, Maestripieri D (2003) Primate rituals: the function of greetings between male Guinea baboons. Ethology 109:847–859Google Scholar
  79. Wittig RM, Crockford C, Weltring A, Langergraber K, Deschner T, Zuberbuehler K (2016) Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations. Nat Commun 7:13361PubMedPubMedCentralGoogle Scholar
  80. Wrangham RW, Smuts BB (1980) Sex differences in the behavioral ecology of chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil 28:13–31Google Scholar
  81. Zuberbuehler K (2005) The phylogenetic roots of language: evidence from primate communication and cognition. Curr Dir Psychol Sci 14:126–130Google Scholar
  82. Zuberbuehler K (2008) Audience effects. Curr Biol 18:R189–R190Google Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Foreign Languages, College of EducationSeoul National UniversityGwanak-guRepublic of Korea
  2. 2.Institute of Cognitive Science, Comparative BiocognitionUniversity OsnabrückOsnabrückGermany

Personalised recommendations