Skip to main content

Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions

Abstract

The ability to recognize conspecifics by their acoustic signals is of crucial importance to social animals, especially where visibility is limited, because it allows for discrimination between familiar and unfamiliar individuals and facilitates associations with and the avoidance of particular conspecifics. Animals may also benefit from an ability to recognize and use the information coded into the auditory signals of other species. Companion species such as dogs, cats, and horses are able to discriminate between familiar and unfamiliar human voices; however, whether this ability is widespread across vertebrates is still unknown. Using playback experiments, we tested whether western gorillas living at Zoo Atlanta were able to discriminate between the voices of subgroups of people: i.e., unfamiliar individuals, familiar individuals with whom the gorillas had positive interactions, and familiar individuals with whom they had negative interactions. Gorillas responded significantly more often (longer gazing duration, higher gazing frequency, shorter latency, and larger number of distress behaviors) to the voices of unfamiliar and familiar-negative individuals than to those of familiar-positive individuals, indicating that they recognized the voices of subgroup of people based on familiarity and possibly the nature of the relationship with them. Future studies should determine whether this is also the case in the wild, where interspecific associations with humans are less intense than they are in captive settings.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10:17–21. https://doi.org/10.1007/s10071-006-0025-8

    Article  PubMed  Google Scholar 

  2. Bakeman R (2005) Recommended effect size statistics for repeated measures designs. Behav Res Methods 37:379–384

    Article  Google Scholar 

  3. Bates LA, Sayialel KN, Njiraini NW, Moss CJ, Poole JH, Byrne RW (2007) Elephants classify human ethnic groups by odor and garment color. Curr Biol 17:1938–1942. https://doi.org/10.1016/j.cub.2007.09.060

    Article  PubMed  CAS  Google Scholar 

  4. Boinski S, Campbell AF (1996) The huh vocalization of white-faced capuchins: a spacing call disguised as a food call? Ethology 102:826–840

    Article  Google Scholar 

  5. Bouchet H, Pellier AS, Blois-Heulin C, Lemasson A (2010) Sex differences in the vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus): a multi-level acoustic analysis. Am J Primatol 72:360–375. https://doi.org/10.1002/ajp.20791

    Article  PubMed  Google Scholar 

  6. Candiotti A, Zuberbuehler K, Lemasson A (2013) Voice discrimination in four primates. Behav Process 99:67–72. https://doi.org/10.1016/j.beproc.2013.06.010

    Article  Google Scholar 

  7. Cheney DL, Seyfarth RM (1996) Function and intention in the calls of non-human primates. Proc Br Acad Lond B Biol Sci 88:59–76

    Google Scholar 

  8. Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367

  9. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, Hillsdale

    Google Scholar 

  10. Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243

    Article  Google Scholar 

  11. Digweed SM, Fedigan LM, Rendall D (2007) Who cares who calls? Selective responses to the lost calls of socially dominant group members in the white-faced capuchin (Cebus capucinus). Am J Primatol 69:829–835

    Article  Google Scholar 

  12. Doran-Sheehy DM, Derby AM, Greer D, Mongo P (2007) Habituation of western gorillas: the process and factors that influence it. Am J Primatol 69:1354–1369. https://doi.org/10.1002/ajp.20442|ISSN0275-2565

    Article  PubMed  Google Scholar 

  13. Dorey N, Conover A, Udell M (2014) Interspecific communication from people to horses (Equus ferus caballus) is influenced by different horsemanship training styles. J Comp Psychol (washington, DC: 1983). https://doi.org/10.1037/a0037255

    Article  Google Scholar 

  14. Driscoll CA, Macdonald DW, O’Brien SJ (2009) From wild animals to domestic pets, an evolutionary view of domestication. PNAS 106(Suppl. 1):9971–9978

    Article  Google Scholar 

  15. Evans TA, Howell S, Westergaard GC (2005) Auditory-visual cross-modal perception of communicative stimuli in Tufted Capuchin Monkeys (Cebus apella). J Exp Psychol Anim Behav Process 31(4):399–406. https://doi.org/10.1037/0097-7403.31.4.399

    Article  PubMed  Google Scholar 

  16. Ey E, Hammerschmidt K, Seyfarth RM, Fischer J (2007a) Age- and sex-related variations in clear calls of Papio ursinus. Int J Primatol 28:947–960. https://doi.org/10.1007/s10764-007-9139-3

    Article  Google Scholar 

  17. Ey E, Pfefferle D, Fischer J (2007b) Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48:253–267

    Article  CAS  Google Scholar 

  18. Fallow P, Magrath R (2010) Eavesdropping on other species: mutual interspecific understanding of urgency information in avian alarm calls. Anim Behav 79:411–417. https://doi.org/10.1016/j.anbehav.2009.11.018

    Article  Google Scholar 

  19. Fichtel C (2004) Reciprocal recognition of sifaka (Propithecus verreauxi verreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls. Anim Cogn 7:45–52. https://doi.org/10.1007/s10071-003-0180-0

    Article  PubMed  Google Scholar 

  20. Ghazanfar AA, Logothetis NK (2003) Facial expressions linked to monkey calls. Nature 423:937–938. https://doi.org/10.1038/423937a

    Article  PubMed  CAS  Google Scholar 

  21. Griffin AS (2004) Social learning about predators: a review and prospectus. Anim Learn Behav 32:131–140. https://doi.org/10.3758/BF03196014

    Article  CAS  Google Scholar 

  22. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. https://doi.org/10.1126/science.1072702

    Article  PubMed  CAS  Google Scholar 

  23. Hare B, Rosati A, Kaminski J, Bräuer J, Call J, Tomasello M (2010) The domestication hypothesis for dogs’ skills with human communication: a response to Udell et al. (2008) and Wynne et al. (2008). Anim Behav 79:e1–e6. https://doi.org/10.1016/j.anbehav.2009.06.031

    Article  Google Scholar 

  24. Hauser MD (1988) How infant vervet monkeys learn to recognize starling alarm calls: the role of experience. Behaviour 105:187–201. https://doi.org/10.1163/156853988x00016

    Article  Google Scholar 

  25. Hedwig D, Mundry R, Robbins MM, Boesch C (2015) Audience effects, but not environmental influences, explain variation in gorilla close distance vocalizations—a test of the acoustic adaptation hypothesis. Am J Primatol 77:1239–1252. https://doi.org/10.1002/ajp.22462

    Article  PubMed  Google Scholar 

  26. Herbinger I, Papworth S, Boesch C, Zuberbühler K (2009) Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Anim Behav 78:1389–1396. https://doi.org/10.1016/j.anbehav.2009.09.010

    Article  Google Scholar 

  27. Hohmann G, Fruth B (1994) Structure and use of distance calls in wild bonobos (Pan paniscus). Int J Primatol 15:767–782

    Article  Google Scholar 

  28. Krebs JR, Dawkins R (1984) Animal signals: mind-reading and manipulation. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 2nd edn. Sinauer, Sunderland, pp 380–402

    Google Scholar 

  29. Kriengwatana B, Escudero P, ten Cate C (2015) Revisiting vocal perception in non-human animals: a review of vowel discrimination, speaker voice recognition, and speaker normalization. Front Psychol. https://doi.org/10.3389/fpsyg.2014.01543

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lampe JF, Andre J (2012) Cross-modal recognition of human individuals in domestic horses (Equus caballus). Anim Cogn 15:623–630. https://doi.org/10.1007/s10071-012-0490-1

    Article  PubMed  Google Scholar 

  31. Lee WY, Han Y-D, Lee S-I, Jablonski PG, Jung J-W, Kim J-H (2016) Antarctic skuas recognize individual humans. Anim Cogn 19:861–865. https://doi.org/10.1007/s10071-016-0970-9

    Article  PubMed  Google Scholar 

  32. Lemasson A, Palombit RA, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035. https://doi.org/10.1007/s00265-007-0530-z

    Article  Google Scholar 

  33. Lemasson A, Remeuf K, Rossard A, Zimmermann E (2012) Cross-taxa similarities in affect-induced changes of vocal behavior and voice in arboreal monkeys. PLoS ONE 7:e45106. https://doi.org/10.1371/journal.pone.0045106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Leroux M, Hetem RS, Hausberger M, Lemasson A (2018) Cheetahs discriminate familiar and unfamiliar human voices. Sci Rep 8:15516. https://doi.org/10.1038/s41598-018-33971-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Levey DJ et al (2009) Urban mockingbirds quickly learn to identify individual humans. Proc Natl Acad Sci 106:8959–8962. https://doi.org/10.1073/pnas.0811422106

    Article  PubMed  PubMed Central  Google Scholar 

  36. Levrero F, Mathevon N (2013) Vocal signature in wild infant chimpanzees. Am J Primatol 75:324–332. https://doi.org/10.1002/ajp.22108

    Article  PubMed  Google Scholar 

  37. Magrath RD, Pitcher BJ, Gardner JL (2009) Recognition of other species’ aerial alarm calls: speaking the same language or learning another? Proc R Soc B Biol Sci 276:769–774. https://doi.org/10.1098/rspb.2008.1368

    Article  Google Scholar 

  38. Marzluff JM, Walls J, Cornell HN, Withey JC, Craig DP (2010) Lasting recognition of threatening people by wild American crows. Anim Behav 79:699–707. https://doi.org/10.1016/j.anbehav.2009.12.022

    Article  Google Scholar 

  39. McComb K, Shannon G, Sayialel KN, Moss C (2014) Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. Proc Natl Acad Sci USA 111:5433–5438. https://doi.org/10.1073/pnas.1321543111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Meise K, Franks DW, Bro-Jorgensen J (2018) Multiple adaptive and non-adaptive processes determine responsiveness to heterospecific alarm calls in African savannah herbivores. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.2676

    Article  Google Scholar 

  41. Mitani JC, Nishida T (1993) Contexts and social correlates of long-distance calling by male chimpanzees. Anim Behav 45:735–746

    Article  Google Scholar 

  42. Muller CA, Manser MB (2008) The information banded mongooses extract from heterospecific alarms. Anim Behav 75:897–904. https://doi.org/10.1016/j.anbehav.2007.07.012

    Article  Google Scholar 

  43. Olejnik S, Algina J (2003) Generalized Eta and Omega squared statistics: measures of effect size for some common research designs. Psychol Methods 8:434–447. https://doi.org/10.1037/1082-989X.8.4.434

    Article  PubMed  Google Scholar 

  44. Ogden JJ, Finlay TW, Maple TL (1990) Gorilla adaptations to naturalistic environments. Zoo Biol 9:107–121. https://doi.org/10.1002/zoo.1430090205

  45. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of “friendships” to female baboons: experimental and observational evidence. Anim Behav 54:599–614

    Article  CAS  Google Scholar 

  46. Papworth S, Milner-Gulland EJ, Slocombe K (2013) Hunted Woolly Monkeys (Lagothrix poeppigii) show threat-sensitive responses to human presence. PLoS ONE. https://doi.org/10.1371/journal.pone.0062000

    Article  PubMed  PubMed Central  Google Scholar 

  47. Pfefferle D, Fischer J (2006) Sounds and size: identification of acoustic variables that reflect body size in hamadryas baboons, Papio Hamadryas. Anim Behav 72:43–51

    Article  Google Scholar 

  48. Pougnault L, Levréro F, Mulot B, Lemasson A (2020) Breaking conversational rules matters to captive gorillas: A playback experiment. Sci Rep 10:6947. https://doi.org/10.1038/s41598-020-63923-7

  49. Proops L, McComb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B Biol Sci 279:3131–3138. https://doi.org/10.1098/rspb.2012.0626

    Article  Google Scholar 

  50. Raemaekers JJ, Raemaekers PM (1985) Field playback of loud calls to gibbons (Hylobates lar)—territorial, sex-specific and species-specific responses. Anim Behav 33:481–493

    Article  Google Scholar 

  51. Rainey HJ, Zuberbühler K, Slater PJB (2004) Hornbills can distinguish between primate alarm calls. Proc R Soc Lond Ser B Biol Sci 271:755–759

    Article  Google Scholar 

  52. Ratcliffe VF, McComb K, Reby D (2014) Cross-modal discrimination of human gender by domestic dogs. Anim Behav 91:127–135. https://doi.org/10.1016/j.anbehav.2014.03.009

    Article  Google Scholar 

  53. Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015

    Article  Google Scholar 

  54. Rendall D, Owren MJ, Weerts E, Hienz RD (2004) Sex differences in the acoustic structure of vowel-like grunt vocalizations in baboons and their perceptual discrimination by baboon listeners. J Acoust Soc Am 115:411–421. https://doi.org/10.1121/1.1635838

    Article  PubMed  Google Scholar 

  55. Saito A, Shinozuka K (2013) Vocal recognition of owners by domestic cats (Felis catus). Anim Cogn 16:685–690. https://doi.org/10.1007/s10071-013-0620-4

    Article  PubMed  Google Scholar 

  56. Salmi R, Doran-Sheehy DM (2014) The function of loud calls (Hoot series) in wild western gorillas (Gorilla gorilla). Am J Phys Anthropol 155:379–391. https://doi.org/10.1002/ajpa.22575

    Article  PubMed  Google Scholar 

  57. Salmi R, Hammerschmidt K, Doran-Sheehy DM (2013) Western gorilla vocal repertoire and contextual use of vocalizations. Ethology 119:831–847. https://doi.org/10.1111/eth.12122

    Article  Google Scholar 

  58. Savage-Rumbaugh S, Sevcik RA, Hopkins WD (1988) Symbolic cross-modal transfer in two species of chimpanzees. Child Dev 59:617–625

    Article  CAS  Google Scholar 

  59. Schmidt KA, Dall SRX, van Gils JA (2010) The ecology of information: an overview on the ecological significance of making informed decisions. Oikos 119:304–316. https://doi.org/10.1111/j.1600-0706.2009.17573.x

    Article  Google Scholar 

  60. Seiler M, Schwitzer C, Gamba M, Holderied MW (2013) Interspecific semantic alarm call recognition in the solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis. PLoS ONE 8:e67397. https://doi.org/10.1371/journal.pone.0067397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Seppänen J-T, Forsman JT, Monkkonen M, Thomson RL (2007) Social information use is a process across time, space, and ecology, reaching heterospecifics. Ecology 88:1622–1633. https://doi.org/10.1890/06-1757.1

    Article  PubMed  Google Scholar 

  62. Seyfarth RM, Cheney DL (1980a) The ontogeny of vervet monkey alarm calling behavior: a preliminary report. Zeitschrift Fuer Tierpsychologie 54:37–56

    Article  Google Scholar 

  63. Seyfarth RM, Cheney DL (1980b) Vocal reocgnition in free ranging vervet monkeys. Anim Behav 28:362–367

    Article  Google Scholar 

  64. Seyfarth RM, Cheney DL (1990) The assessment by vervet monkeys of their own and another species’ alarm calls. Anim Behav 40:754–764

    Article  Google Scholar 

  65. Seyfarth RM, Cheney DL (2008) The evolution of social categories. In: Bethoz A, Christen Y (eds) Neurobiology of “umwelt”: how living beings perceive the world. Springer, Berlin, pp 69–87

    Google Scholar 

  66. Seyfarth RM, Cheney DL (2012) Social relationships, social cognition, and the evolution of mind in primates. In: Handbook of psychology, 2nd edn. https://doi.org/10.1002/9781118133880.hop203021

  67. Shriner WM (1998) Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm calls. Anim Behav 55:529–536. https://doi.org/10.1006/anbe.1997.0623

    Article  PubMed  CAS  Google Scholar 

  68. Sliwa J, Duhamel J-R, Pascalis O, Wirth S (2011) Spontaneous voice-face identity matching by rhesus monkeys for familiar conspecifics and humans. Proc Natl Acad Sci USA 108:1735–1740. https://doi.org/10.1073/pnas.1008169108

    Article  PubMed  PubMed Central  Google Scholar 

  69. Stephan C, Wilkinson A, Huber L (2012) Have we met before? Pigeons recognise familiar human faces. Avian Biol Res 5:75–80. https://doi.org/10.3184/175815512x13350970204867

    Article  Google Scholar 

  70. Struhsaker TT (1981) Polyspecific associations among tropical rain-forest primates. Z Tierpsychol 57:268–304. https://doi.org/10.1111/j.1439-0310.1981.tb01928.x

    Article  Google Scholar 

  71. Tomczak A, Tomczak E (2014) The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends Sport Sci 1:19–25

  72. Uster D, Zuberbühler K (2001) The functional significance of Diana monkey “clear” calls. Behaviour 138:741–756

    Article  Google Scholar 

  73. Ward P, Zahavi A (1973) The importance of certain assemblages of birds as ‘Information-Centres’ for food finding. Ibis 115:517–534

    Article  Google Scholar 

  74. Wascher CAF, Szipl G, Boeckle M, Wilkinson A (2012) You sound familiar: carrion crows can differentiate between the calls of known and unknown heterospecifics. Anim Cogn 15:1015–1019. https://doi.org/10.1007/s10071-012-0508-8

    Article  PubMed  PubMed Central  Google Scholar 

  75. Waser PM (1975) Experimental playbacks show vocal mediation of intergroup avoidance in a forest monkey. Nature 255:56–58

    Article  Google Scholar 

  76. Weiss DJ, Garibaldi BT, Hauser MD (2001) The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. J Comp Psychol 115:258–271

    Article  CAS  Google Scholar 

  77. Wich SA, Assink PR, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): the effect of familiarity. Behaviour 139:79–87. https://doi.org/10.1163/15685390252902292

  78. Wich SA, Sterck EHM (2007) Familiarity and threat of opponents determine variation in Thomas langur (Presbytis thomasi) male behaviour during between-group encounters. Behaviour 144:1583–1598. https://doi.org/10.1163/156853907782512065

    Article  Google Scholar 

  79. Zayan R, Vauclair J (1998) Categories as paradigms for comparative cognition. Behav Proc 42:87–99. https://doi.org/10.1016/S0376-6357(97)00064-8

    Article  CAS  Google Scholar 

  80. Zuberbühler K (2000) Interspecies semantic communication in two forest primates. Proc R Soc Lond Ser B Biol Sci 267:713–718

    Article  Google Scholar 

Download references

Acknowledgements

We thank all the Zoo Atlanta workers (caregivers, veterinarians, and maintenance staff) and UGA employees who agreed to have their voices recorded. We are particularly grateful to the gorilla caregivers who helped us logistically with this project, and to the gorillas who participated in this study. We thank Haleigh Randazzo, who co-coded the videos, and the Center for Geospatial Research for the use of video equipment. The project was funded by the University of Georgia and through The Experiment Crowdsource Platform. We would like to personally thank Douglas Murray, Alex Piel, Ari Grossman, Manuela Nanni, Barbara Orelli, Lynne LaVallee, David, Ashley Sullivan, Stacy Watts, Marc Myers, Wendy M. Erb, Eileen Larney, Theresa R. Jones, Debbie Copan, Edwin Watts, Jade Schmitt, Tara Stoinski, Cristiano Marinucci, Jessica Lodwick, S. R. Batchelder, Cindy Maupin, Cornelia Seiffert, Patti L. R., Kerry Ossi-Lupo, Stacy Eason, Cara N. Love, Donita Schultz, John Boone, Natalie Schwob, Alexis Stern, Christina Doyle Sheehan, Linda Fabiani, Cherri Cherri, Jan Gogarten, Anja Deppe, Raymond Vagell, Fabrizio Salmi, Eric D. Walters, and a few more anonymous supporters for their donations. Our research protocol was approved by the Zoo Atlanta Scientific Review and by the Committee Institutional Animal Care and Use Committee of the University of Georgia and adhered to the Code of Best Practices for Field Primatology of the International Primatological Society and the American Society of Primatology.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Roberta Salmi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 5013 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Salmi, R., Jones, C.E. & Carrigan, J. Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions. Anim Cogn (2021). https://doi.org/10.1007/s10071-021-01543-y

Download citation

Keywords

  • Heterospecific vocal recognition
  • Ape communication
  • Gorilla gorilla
  • Heterospecific eavesdropping