Advertisement

Wild vervet monkeys copy alternative methods for opening an artificial fruit

Abstract

Experimental studies of animal social learning in the wild remain rare, especially those that employ the most discriminating tests in which alternative means to complete naturalistic tasks are seeded in different groups. We applied this approach to wild vervet monkeys (Chlorocebus aethiops) using an artificial fruit (‘vervetable’) opened by either lifting a door panel or sliding it left or right. In one group, a trained model lifted the door, and in two others, the model slid it either left or right. Members of each group then watched their model before being given access to multiple baited vervetables with all opening techniques possible. Thirteen of these monkeys opened vervetables, displaying a significant tendency to use the seeded technique on their first opening and over the course of the experiment. The option preferred in these monkeys’ first successful manipulation session was also highly correlated with the proportional frequency of the option they had previously witnessed. The social learning effects thus documented go beyond mere stimulus enhancement insofar as the same door knob was grasped for either technique. Results thus suggest that through imitation, emulation or both, new foraging techniques will spread across groups of wild vervet monkeys to create incipient foraging traditions.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aplin LM, Sheldon BC, Morand-Ferron J (2013) Milk bottles revisited: social learning and individual variation in the blue tit (Cyanistes caeruleus). Anim Behav 85:1225–1232. doi:10.1016/j.anbehav.2013.03.009

  2. Bugnyar T, Huber L (1997) Push or pull: an experimental study on marmosets. Anim Behav 54:817–831. doi:10.1006/anbe.1996.0497

  3. Buttelmann D, Carpenter M, Call J, Tomasello M (2007) Enculturated chimpanzees imitate rationally. Dev Sci 1:31–38. doi:10.1111/j.1467-7687.2007.00630.x

  4. Claidière N, Whiten A (2012) Integrating the study of conformity and culture in humans and nonhuman animals. Psychol Bull 138(1):126–145. doi:10.1037/a0025868

  5. Dawson BV, Foss BM (1965) Observational learning in budgerigars. Anim Behav 13:470–474

  6. Dindo M, Thierry B, Whiten A (2008) Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc R Soc B 275:187–193. doi:10.1098/rspb.2007.1318

  7. Dindo M, de Waal FBM, Whiten A (2009) In-group conformity sustains different foraging traditions in capuchin monkeys (Cebus apella). PLoS One 4:e7858. doi:10.1371/journal.pone.0007858

  8. Fuhrmann D, Ravignani A, Marshall-Pescini S, Whiten A (2014) Synchrony and motor mimicking in chimpanzee observational learning. Sci Rep 4:5283. doi:10.1038/srep05383

  9. Galef BG Jr, Allen C (1995) A new model system for studying animal tradition. Anim Behav 50:705–717. doi:10.1016/0003-3472(95)80131-6

  10. Gunhold T, Massen JJM, Schiel N, Souto A, Bugnyar T (2014a) Memory, transmission and persistence of alternative foraging techniques in wild common marmosets. Anim Behav 91:79–91. doi:10.1016/j.anbehav.2014.02.023

  11. Gunhold T, Whiten A, Bugnyar T (2014b) Video demonstrations seed alternative problem-solving techniques in wild common marmosets. Biol Lett 10(9):20140439. doi:10.1098/rsbl.2014.0439

  12. Helfman GS, Schultz ET (1984) Social transmission of behavioural traditions in a coral reef fish. Anim Behav 32:379–384

  13. Henrich J, Broesch J (2011) On the nature of cultural transmission networks: evidence from Fijian villages for adaptive learning biases. Philos Trans R Soc B 366(1567):1139–1148

  14. Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69(2):207–231

  15. Hopper LM, Spiteri A, Lambeth SP, Schapiro SJ, Horner V, Whiten A (2007) Experimental studies of traditions and underlying transmission processes in chimpanzees. Anim Behav 73:1021–1032. doi:10.1016/j.anbehav.2006.07.016

  16. Hopper LM, Lambeth SP, Schapiro SJ, Whiten A (2008) Observational learning in chimpanzees and children studied through ‘ghost’ conditions. Proc R Soc Lond B 275:835–840. doi:10.1098/rspb.2007.1542

  17. Hoppitt W, Laland KN (2008) Social processes influencing learning in animals: a review of the evidence. Adv Study Behav 38:105–165. doi:10.1016/S0065-3454(08)00003-X

  18. Hoppitt W, Laland KN (2013) Social learning: an introduction to mechanisms, methods and models. Princeton University Press, Princeton

  19. Horner V, Whiten A, Flynn EG, de Waal FBM (2006) Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proc Natl Acad Sci USA 103:13878–13883. doi:10.1073/pnas.0606015103

  20. Horner V, Proctor D, Bonnie KE, Whiten A, de Waal FBM (2010) Prestige affects cultural learning in chimpanzees. PLoS One 5(5):e10625. doi:10.1371/journal.pone.0010625

  21. Jaeggi AV, Dunkel LP, Van Noordwijk MA, Wich SA, Sura AA, van Schaik CP (2010) Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture. Am J Primatol 72(1):62–71. doi:10.1002/ajp.20752

  22. Kendal RL, Galef BG, van Schaik CP (2010a) Social learning research outside the laboratory: how and why? Learn Behav 38:187–194. doi:10.3758/LB.38.3.187

  23. Kendal RL, Custance DM, Kendal JR, Vale G, Stoinski TS, Rakotomalala NL, Rasamimanana H (2010b) Evidence for social learning in wild lemurs (Lemur catta). Learn Behav 38:220–234. doi:10.3758/LB.38.3.220

  24. Kendal R, Hopper LM, Whiten A, Brosnan SF, Lambeth SP, Schapiro SJ, Hoppitt W (2014) Chimpanzees copy dominant and knowledgeable individuals: implications for cultural diversity. Evol Hum Behav. doi:10.1016/j.evolhumbehav.2014.09.002

  25. Langen TA (1996) Social learning of a novel foraging skill by white-throated magpie-jays (Calocitta formosa, Corvidae): a field experiment. Ethology 102:157–166

  26. Lefebvre L (1986) Cultural diffusion of a novel food-finding behaviour in urban pigeons: an experimental field test. Ethology 71:295–304

  27. Lonsdorf EV, Eberly LE, Pusey AE (2004) Sex differences in learning in chimpanzees. Nature 428(6984):715–716. doi:10.1038/428715a

  28. Nielsen M, Subiaul F, Galef BG Jr, Zentall TR, Whiten A (2012) Social learning in humans and non-humans animals: theoretical and empirical dissections. (Introduction to special issue). J Comp Psychol 126:109–113. doi:10.1037/a0027758

  29. Panger MA, Perry S, Rose L, Gros-Luis J, Vogel E, Mackinnon KC, Baker M (2002) Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus). Am J Phys Anthropol 119:52–56. doi:10.1002/ajpa.10103

  30. Perry S (2009) Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus). Anim Cogn 12:705–716. doi:10.1007/s10071-009-0230-3

  31. Price E, Caldwell CA (2007) Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis. Behav Process 74:13–20. doi:10.1016/j.beproc.2006.09.003

  32. Rawlings B, Davila-Ross M, Boysen ST (2014) Semi-wild chimpanzees open hard-shelled fruits differently across communities. Anim Cogn 17(4):891–899. doi:10.1007/s10071-013-0722-z

  33. Reader SM, Biro D (2010) Experimental identification of social learning in wild animals. Learn Behav 38(3):265–283. doi:10.1016/j.evolhumbehav.2011.11.010

  34. Renevey N, Bshary R, van de Waal E (2013) Philopatric vervet monkey females are the focus of social attention rather independently of rank. Behaviour 150:599–615. doi:10.1163/1568539X-00003072

  35. Santorelli CJ, Schaffner CM, Campbell CJ, Notman H, Pavelka MS, Weghorst JA, Aureli F (2011) Traditions in spider monkeys are biased towards the social domain. PLoS One 6:e16863. doi:10.1371/journal.pone.0016863

  36. Schnoell AV, Fichtel C (2012) Wild redfronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Anim Cogn 15:505–516. doi:10.1007/s10071-012-0477-y

  37. Schnoell AV, Dittmann MT, Fichtel C (2014) Human-introduced long-term traditions in wild redfronted lemurs? Anim Cogn 17(1):45–54. doi:10.1007/s10071-013-0636-9

  38. Sigg H (1980) Differentiation of Female Positions in Hamadryas One-Male-Units. Z Tierpsychol 53(3):265–302

  39. R Core Team (2013) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org/

  40. Tennie C, Call J, Tomasello M (2009) Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans R Soc B 364(1528):2405–2415. doi:10.1098/rstb.2009.0052

  41. Tennie C, Call J, Tomasello M (2010) Evidence for emulation in chimpanzees in social settings using the floating peanut task. PLoS One 5(5):e10544. doi:10.1371/journal.pone.0010544

  42. Thornton A, Clutton-Brock T (2011) Social learning and the development of individual and group behaviour in mammal societies. Philos Trans R Soc B 366:978–987. doi:10.1098/rstb.2010.0312

  43. Thornton A, Malapert A (2009) Experimental evidence for social transmission of food acquisition techniques in wild meerkats. Anim Behav 78:255–264. doi:10.1016/j.anbehav.2009.04.021

  44. Thorpe WH (1963) Learning and instinct in animals, 2nd edn. Methuen, London

  45. Tomasello M (1990) Cultural transmission in tool use and communicatory signalling of chimpanzees. In: Parker S, Gibson K (eds) “Language” and intelligence in monkeys and apes: Comparative developmental perspectives. Cambridge University Press, Cambridge, pp 274–311

  46. Tomasello M (1996) Do apes ape? In: Heyes CM, Galef BG (eds) Social learning in animals: the roots of culture. Academic Press, London, pp 319–346

  47. van de Waal E, Bshary R (2011) Social learning abilities of wild vervet monkeys in a two-step task artificial fruit experiment. Anim Behav 81:433–438. doi:10.1016/j.anbehav.2010.11.013

  48. van de Waal E, Whiten A (2012) Spontaneous emergence, imitation and spread of alternative foraging techniques among groups of vervet monkeys. PLoS One 7(10):e47008. doi:10.1371/journal.pone.0047008

  49. van de Waal E, Renevey N, Favre CM, Bshary R (2010) Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc R Soc B 277:2105–2111. doi:10.1098/rspb.2009.2260

  50. van de Waal E, Krützen M, Hula J, Goudet J, Bshary B (2012) Similarity in food cleaning techniques within matrilines in wild vervet monkeys. PLoS One 7(4):e35694. doi:10.1371/journal.pone.0035694

  51. van de Waal E, Claidière N, Whiten A (2013a) Social learning and spread of alternative means of opening an artificial food in four groups of vervet monkeys (Chlorocebus aethiops). Anim Behav 85:71–76. doi:10.1016/j.anbehav.2012.10.008

  52. van de Waal E, Borgeaud C, Whiten A (2013b) Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340(6131):483–485. doi:10.1126/science.1232769

  53. van de Waal E, Bshary R, Whiten A (2014) Wild vervet monkey infants acquire the food-processing variants of their mothers. Anim Behav 90:41–45. doi:10.1016/j.anbehav.2014.01.015

  54. van Leeuwen EJ, Cronin KA, Haun DB (2014) A group-specific arbitrary tradition in chimpanzees (Pan troglodytes). Anim Cogn 17(6):1421–1425. doi:10.1007/s10071-014-0766-8

  55. van Schaik CP, Ancrenaz M, Borgen G, Galdikas B, Knott CD, Singleton I, Suzuki A, Utami SS, Merrill M (2003) Orangutan cultures and the evolution of material culture. Science 299:102–105. doi:10.1126/science.1078004

  56. Visalberghi E, Fragaszy DM (2002) Do monkeys ape?—Ten years after. In: Dautenhahn K, Nehaniv CL (eds) Imitation in animals and artifacts. MIT Press, Cambridge, pp 471–499

  57. Voelkl B, Huber L (2000) True imitation in marmosets. Anim Behav 60:195–202. doi:10.1006/anbe.2000.1457

  58. Warner RR (1988) Traditionality of mating site preferences in a coral reef fish. Nature 335:719–721. doi:10.1038/335719a0

  59. Whiten A (1998) Imitation of the sequential structure of actions by chimpanzees (Pan troglodytes). J Comp Psychol 112:270–281

  60. Whiten A (2012) Social learning, traditions and culture. In: Mitani J, Call J, Kappeler P, Palombit P, Silk J (eds) The evolution of primate societies. Chicago University Press, Chicago, pp 681–699

  61. Whiten A, Flynn E (2010) The transmission and evolution of experimental microcultures in groups of young children. Dev Psychol 46(6):1694–1709. doi:10.1037/a0020786

  62. Whiten A, Ham R (1992) On the nature and evolution of imitation in the animal kingdom: reappraisal of a century of research. Adv Study Behav 11:239–283

  63. Whiten A, Mesoudi A (2008) Establishing an experimental science of culture: animal social diffusion experiments. Philos Trans R Soc B 363:3477–3488. doi:10.1098/rstb.2008.0134

  64. Whiten A, Custance DM, Gomez JC, Teixidor P, Bard KA (1996) Imitative learning of artificial fruit processing in children (Homo sapiens) and chimpanzees (Pan troglodytes). J Comp Psychol 110:3–14. doi:10.1037/0735-7036.110.1.3

  65. Whiten A, Horner V, Litchfield C, Marshall-Pescini S (2004) How do apes ape? Learn Behav 32:36–52. doi:10.3758/BF03196005

  66. Whiten A, Horner V, de Waal FBM (2005) Conformity to cultural norms of tool use in Chimpanzees. Nature 437:737–740. doi:10.1038/nature04047

  67. Whiten A, Spiteri A, Horner V, Bonnie KE, Lambeth SP, Schapiro SJ, de Waal FBM (2007) Transmission of multiple traditions within and between chimpanzee groups. Curr Biol 17:1038–1043. doi:10.1016/j.cub.2007.05.031

  68. Whiten A, McGuigan N, Marshall-Pescini S, Hopper LM (2009) Emulation, imitation, overimitation and the scope of culture for child and chimpanzee. Philos Trans R Soc B 364:2417–2428. doi:10.1098/rstb.2009.0069

  69. Whiten A, Hinde RA, Laland KN, Stringer CB (2011) Culture evolves. Philos Trans R Soc B 366:938–948. doi:10.1098/rstb.2010.0372

  70. Wood D (1989) Social interaction as tutoring. In: Bornstein MH, Bruner JS (eds) Interaction in human development. Erlbaum, Hillsdale, pp 59–80

  71. Zentall TR (2012) Perspectives on social learning in animals. J Comp Psychol 126:114–128. doi:10.1037/a0025381

  72. Zentall TR, Sutton JE, Sherburne LM (1996) True imitative learning in pigeons. Psychol Sci 7:343–346. doi:10.1111/j.1467-9280.1996.tb00386.x

Download references

Acknowledgments

This project was supported by a Sinergia grant (CRSI33_133040) from the Swiss National Science Foundation to R. Bshary, C. P. van Schaik and A. Whiten, and by a SNSF personal grant of E.W. (P300P3_151187). We are particularly grateful to Kerneels van der Walt for permission to conduct the study in his reserve and Albert Driescher for his vital support in the field. The study was registered with Ezemvelo KZN Wildlife in South Africa and gained approval from the Ethics Committee of the School of Psychology and Neuroscience, University of St Andrews. We are grateful to all IVP field team for assistance in data collection during experimental sessions. Thanks to Andy Burnley for constructing the vervetables. We are grateful to Tina Gunhold for useful comments on the manuscript.

Author information

Correspondence to Andrew Whiten.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Video 1 Lift opening of the vervetable during demonstration phase (Baie Dankie group). (MPG 3544 kb)

Video 2 Slide to the right opening of the vervetable during demonstration phase (Ankhase group). (MPG 1748 kb)

Video 1 Lift opening of the vervetable during demonstration phase (Baie Dankie group). (MPG 3544 kb)

Video 2 Slide to the right opening of the vervetable during demonstration phase (Ankhase group). (MPG 1748 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

van de Waal, E., Claidière, N. & Whiten, A. Wild vervet monkeys copy alternative methods for opening an artificial fruit. Anim Cogn 18, 617–627 (2015) doi:10.1007/s10071-014-0830-4

Download citation

Keywords

  • Field experiments
  • Social learning
  • Imitation
  • Cultural transmission
  • Primates
  • Vervet monkeys