Abstract
Comparative experimental studies of imitative learning have focused mainly on primates and birds. However, cetaceans are promising candidates to display imitative learning as they have evolved in socioecological settings that have selected for large brains, complex sociality, and coordinated predatory tactics. Here we tested imitative learning in killer whales, Orcinus orca. We used a ‘do-as-other-does’ paradigm in which 3 subjects witnessed a conspecific demonstrator’s performance that included 15 familiar and 4 novel behaviours. The three subjects (1) learned the copy command signal ‘Do that’ very quickly, that is, 20 trials on average; (2) copied 100 % of the demonstrator’s familiar and novel actions; (3) achieved full matches in the first attempt for 8–13 familiar behaviours (out of 15) and for the 2 novel behaviours (out of 2) in one subject; and (4) took no longer than 8 trials to accurately copy any familiar behaviour, and no longer than 16 trials to copy any novel behaviour. This study provides experimental evidence for body imitation, including production imitation, in killer whales that is comparable to that observed in dolphins tested under similar conditions. These findings suggest that imitative learning may underpin some of the group-specific traditions reported in killer whales in the field.
Similar content being viewed by others
References
Baird RW (2000) The killer whale: foraging specializations and group hunting. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 127–153
Barrett-Lennard LG, Heise K (2007) The natural history and ecology of killer whales: foraging specialization in a generalist predator. In: Estes JA, Brownell RL, DeMaster DP, Doak DF, Williams TM (eds) Whales, whaling and ocean ecosystems. University of California Press, Berkely, pp 163–173
Bates LA, Byrne RW (2010) Imitation: what animal imitation tells us about animal cognition. Wiley Interdiscip Rev Cogn Sci 1:685–695. doi:10.1002/wcs.77
Bauer GB, Johnson CM (1994) Trained motor imitation by bottlenosed dolphins (Tursiops truncatus). Percept Mot Skills 79:1307–1315
Bigg MA, Olesiuk PF, Ellis GM, Ford JKB, Balcomb KC (1990) Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Rep Int Whal Commn 12:383–405
Byrne RW (2002) Imitation of novel complex actions: what does the evidence from animals mean? Adv Study Behav 31:77–105. doi:10.1016/S0065-3454(02)80006-7
Byrne RW (2009) Animal imitation. Curr Biol 19:R111–R114
Byrne RW, Russon AE (1998) Learning by imitation: a hierarchical approach. Behav Brain Sci 21:667–684. doi:10.1017/S0140525X98001745
Caldwell CA, Whiten A (2002) Evolutionary perspectives on imitation: is a comparative psychology of social learning possible? Anim Cogn 5:193–208. doi:10.1007/s10071-002-0151-x
Call J (2001) Body imitation in an enculturated orangután (Pongo pygmaeus). Cybern Syst 32:97–119. doi:10.1080/019697201300001821
Call J, Tomasello M (1996) The effect of humans on the cognitive development of apes. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought. Cambridge University Press, New York, pp 371–403
Caro TM, Hauser MD (1992) Is there teaching in nonhuman animals? Q Rev Biol 67:151–174. doi:10.1086/417553
Carpenter M (2006) Instrumental, social, and shared goals and intentions in imitation. In: Rogers SJ, Williams J (eds) Imitation and the development of the social mind: lessons from typical development and autism. Guilford, New York, pp 48–70
Carpenter M, Call J (2009) Comparing the imitative skills of children and nonhuman apes. Revue de Primatologie 1(1). See http://primatologie.revues.org/263
Carrasco L, Posada S, Colell M (2009) New evidence on imitation in an encultured chimpanzee (Pan troglodytes). J Comp Psychol 123(4):385–390. doi:10.1037/a0016275
Custance DA, Whiten A, Bard KA (1995) Can young chimpanzees imitate arbitrary actions? Hayes and Hayes (1952) revisited. Behaviour 132:839–858. doi:10.1163/156853995X00036
Deecke VB, Ford JKB, Spong P (2000) Dialect change in resident killer whales: implications for vocal learning and cultural transmission. Anim Behav 40:629–638. doi:10.1006/anbe.2000.1454
Deecke VB, Barrett-Lennard LG, Spong P, Ford JKB (2010) The structure of stereotyped calls reflects kinship and social affiliation in resident killer whales (Orcinus orca). Naturwissenschaften 97:513–518. doi:10.1007/s00114-010-0657-z
Ford JKB (1991) Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can J Zool 69:1454–1483. doi:10.1139/z91-206
Galef BG (2001) Where is the beef? Evidence of culture, imitation and teaching in cetaceans? Behav Brain Sci 24:335. doi:10.1017/S0140525X01343960
Galef BG (2009) Culture in animals? In: Laland KN, Galef BG (eds) The question of animal culture. Harvard University Press, Cambridge, pp 222–246
Gergely G, Csibra G (2006) Sylvia’s recipe: the role of imitation and pedagogy in the transmission of human culture. In: Enfield NJ, Levinson SC (eds) Roots of human sociality: culture, cognition, and human interaction. Berg Publishers, Oxford, pp 229–255
Guinet C (1991) Intentional stranding apprenticeship and social play in killer whales (Orcinus orca). Can J Zool 69:2712–2716
Guinet C, Bouvier J (1995) Development of intentional stranding hunting techniques in killer whale (Orcinus orca) calves at Crozet Archipelago. Can J Zool 73:27–33
Guinet C, Domenici P, de Stephanis R, Barrett-Lennard LG, Ford JKB, Verborgh P (2007) Killer whale predation on bluefin tuna: exploring the hypothesis of the endurance-exhaustion technique. Mar Ecol Prog Ser 347:111–119
Herman LM (2002) Vocal, social, and self-imitation by bottlenosed dolphins. In: Dautenhahn K, Nehaniv C (eds) Imitation in animals and artifacts. MIT Press, Cambridge, pp 63–108
Herman LM (2006) Intelligence and rational behaviour in the bottlenosed dolphin. In: Hurley S, Nudds M (eds) Rational animals? Oxford University Press, Oxford, pp 439–467
Herman LM (2010) What laboratory research has told us about dolphin cognition. Int J Comp Psychol 23:310–330
Herman LM, Pack AA, Morrel-Samuels P (1993) Representational and conceptual skills of dolphins. In: Roitblat HR, Herman LM, Nachtigall P (eds) Language and communication: comparative perspectives. Lawrence Erlbaum, Hillside, pp 273–298
Heyes CM (2012) What can imitation do for cooperation? In: Calcott B, Joyce R, Stereiny K (eds) Signalling, commitment and cooperation. MIT Press, Cambridge (in press)
Huber L, Range F, Voelkl B, Szucsich A, Viranyi Z, Miklosi A (2009) The evolution of imitation: what do the capacities of nonhuman animals tell us about the mechanisms of imitation? Philos Trans R Soc Lond B Biol Sci 364:2299–2309
Jaakkola K, Guarino E, Rodriguez M (2010) Blindfolded imitation in a bottlenose dolphin (Tursiops truncatus). Int J Comp Psychol 23:671–688
Laland KN, Galef BG (2009) The question of animal culture. Harvard University Press, Cambridge
Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547. doi:10.1016/j.tree.2006.06.005
Lopez JC, Lopez D (1985) Killer whales of Patagonia and their behaviour of intentional stranding while hunting nearshore. J Mammal 66:181–183
Marino L (2002) Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav Evol 59:21–32. doi:10.1371/journal.pbio.0050139
Marino L (2004) Dolphin cognition. Curr Biol 14:910–911
Marino L, Connor RC, Fordyce RE, Herman LM, Hof PR et al (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5(966–972):e139. doi:10.1371/journal.pbio.0050139
Matkin CO, Matkin DR, Ellis GM, Saulitis E, McSweeney D (1997) Movements of resident killer whales in southeastern Alaska and Prince William Sound, Alaska. Mar Mammal Sci 13(3):469–475. doi:10.1111/j.1748-7692.1997.tb00653.x
Meltzoff AN, Decety J (2003) What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. Phil Trans R Soc B 358:491–500. doi:10.1098/rstb.2002.1261
Mercado E III, Murray SO, Uyeyama RK, Pack AA, Herman LM (1998) Memory for recent actions in the bottlenosed dolphin (Tursiops truncatus): repetition of arbitrary behaviors using an abstract rule. Anim Learn Behav 26:210–218
Moore BR (1992) Avian movement imitation and a new form of mimicry: tracing the evolution of a complex form of learning. Behaviour 122:231–263. doi:10.1163/156853992X00525
Myowa-Yamakoshi M, Matsuzawa T (1999) Factors influencing imitation of manipulatory actions in chimpanzees (Pan troglodytes). J Comp Psychol 113:128–136. doi:10.1037/0735-7036.113.2.128
Osborne RW (1986) A behavioural budget of Puget Sound killer whales. In: Kirkevold BC, Lockard JS (eds) Behavioural biology of killer whales. Liss AR Inc., New York, pp 211–249
Pitman RL, Durban JW (2012) Cooperative hunting behaviour, prey selectivity and prey handling by pack ice killer whales (Orcinus orca), type B, in Antarctic Peninsula waters. Mar Mammal Sci 28:16–36. doi:10.1111/j.1748-7692.2010.00453.x
Rendell L, Whitehead H (2001) Culture in whales and dolphins. Behav Brain Sci 24: 309–324 (discussion 324–382). doi:10.1017/S0140525X0100396X
Richards DG (1986) Dolphin vocal mimicry and vocal object labelling. In: Schusterman RJ, Thomas JA, Wood FG (eds) Dolphin cognition and behavior: a comparative approach. Lawrence Erlbaum Associates Inc., Hillsdale
Richards DG, Wolz JP, Herman LM (1984) Vocal mimicry of computer-generated sounds and vocal labelling of objects by bottlenose dolphins (Tursiops truncatus): evidence for vocal learning. J Comp Psychol 98:10–28
Riesch R, Barrett-Lennard LG, Ellis GM, Ford JKB, Deecke VB (2012) Cultural traditions and the evolution of reproductive isolation: ecological speciation in killer whales? Biol J Linn Soc 106(1):1–17
Sargeant B, Mann J (2009) Developmental evidence for foraging traditions in wild bottlenose dolphins. Anim Behav 78:715–721
Similä T, Ugarte F (1993) Surface and underwater observation of cooperatively feeding killer whales in Northern Norway. Can J Zool 71:1494–1499
Smith TG, Siniff DB, Reichle R, Stone S (1981) Coordinated behavior of killer whales, (Orcinus orca), hunting a crabeater seal, (Lobodon carcinophagus). Can J Zool 59:1185–1189
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
Tomasello M (1999) The cultural origins of human cognition. Harvard University Press, Cambridge
Tomasello M (2009) The question of chimpanzee culture, plus postscript (chimpanzee culture 2009). In: Laland KN, Galef BG (eds) The question of animal culture. Harvard University Press, Cambridge, pp 198–221
Tomasello M, Kruger AC, Ratner HH (1993) Cultural learning. Behav Brain Sci 16:495–511
Topal J, Byrne RW, Miklosi A, Csanyi V (2006) Reproducing human actions and action sequences: ‘do as I do!’ in a dog. Anim Cogn 9:355–367
Visser IN (1999) Benthic foraging on stingrays by killer whales (Orcinus orca) in New Zealand waters. Mar Mammal Sci 15:220–227
Weiß BM, Symonds H, Spong P, Ladich F (2010) Call sharing across vocal clans of killer whales: evidence for vocal imitation? Mar Mammal Sci 27(2):E1–E13. doi:10.1111/j.1748-7692.2010.00397
Whitehead H (2009) How might we study culture? A perspective from the ocean. In: Laland KN, Galef BG (eds) The question of animal culture. Harvard University Press, Cambridge, pp 125–151
Whiten A (2000) Primate culture and social learning. Cog Sci 24:477–508
Xitco MJ (1988) Mimicry of modeled behaviours by bottlenose dolphins. Unpublished Master of Science thesis, University of Hawaii, Honolulu
Yeater D, Kuczaj SA (2010) Observational learning in wild and captive dolphins. Int J Comp Psychol 23(3):379–385
Yurk H (2003) Do killer whales have culture? In: de Waal FBM, Tyack PL (eds) Animal social complexity. Harvard University Press, Cambridge, pp 465–469
Yurk H, Barrett-Lennard L, Ford JKB, Matkin CO (2002) Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Anim Behav 63:1103–1119. doi:10.1006/anbe.2002.3012
Zentall TR (2006) Imitation: definitions, evidence, and mechanisms. Anim Cogn 9:335–353. doi:10.1007/s10071-006-0039-2
Acknowledgments
Research reported in this study was partly supported by a FPI studentship to José Z. Abramson, and by project grants CCG08-UCM/SAL-4007 (Universidad Complutense de Madrid y Comunidad de Madrid) to V. Hernández-Lloreda, and UCM- BSCH GR58/08 (Universidad Complutense de Madrid y Banco Santander Central Hispano) and D/018712/08 AECID (Agencia Española de Cooperación Internacional y Desarrollo), Spain, to F. Colmenares. We are grateful to the directors of Parques Reunidos and the Marineland Aquarium of Antibes, Jesús Fernández, Jon Kershaw, and Manuel García Hartmann, for allowing us to conduct this research. Furthermore, we appreciate the work and especially thank head coach Lindsay Rubinacam, and all orca trainers team for their help and support. Special thanks go to Titaví for her artwork.
Conflict of interest
The authors declared that they had no conflicts of interest with respect to their authorship and/or the publication of this article.
Ethical standards
This research adhered to the legal requirements of the country (France) in which the work was carried out and all institutional guidelines.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 1 (MPG 6982 kb)
Supplementary material 2 (MPG 3894 kb)
Supplementary material 3 (MPG 5446 kb)
Supplementary material 4 (MPG 11137 kb)
Supplementary material 5 (MPG 5398 kb)
Rights and permissions
About this article
Cite this article
Abramson, J.Z., Hernández-Lloreda, V., Call, J. et al. Experimental evidence for action imitation in killer whales (Orcinus orca). Anim Cogn 16, 11–22 (2013). https://doi.org/10.1007/s10071-012-0546-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-012-0546-2