Animal Cognition

, Volume 16, Issue 2, pp 233–240 | Cite as

Contagious yawning in domestic dog puppies (Canis lupus familiaris): the effect of ontogeny and emotional closeness on low-level imitation in dogs

  • Elainie Alenkær MadsenEmail author
  • Tomas Persson
Original Paper


Contagious yawning is a well-documented phenomenon in humans and has recently attracted much attention from developmental and comparative sciences. The function, development and underlying mechanisms of the phenomenon, however, remain largely unclear. Contagious yawning has been demonstrated in dogs and several non-human primate species, and theoretically and empirically associated with empathy in humans and non-human primates. Evidence of emotional closeness modulating contagious yawning in dogs has, nonetheless, been contradictory. Humans show a developmental increase in susceptibility to yawn contagion, with typically developing children displaying a substantial increase at the age of four, when a number of cognitive abilities (e.g. accurate identification of others’ emotions) begin to clearly manifest. Explicit tests of yawn contagion in non-human animals have, however, thus far only involved adult individuals. Here, we report a study of the ontogeny of domestic dogs’ (Canis lupus familiaris) susceptibility to yawn contagion, and whether emotional closeness to the yawning model affects this. Thirty-five dogs, aged 4–14 months, observed a familiar and unfamiliar human repeatedly yawn or gape. The dogs yawned contagiously, but emotional closeness with the model did not affect the strength of contagion, raising questions as to recent evidence of emotionally modulated auditory contagious yawning in dogs. The dogs showed a developmental effect, with only dogs above 7 months evidencing contagion. The results support the notion of a developmental increase in dogs’ attention to others and identification of others’ emotional states and suggest that yawn contagion is underpinned by developmental processes shared by humans and other animals.


Canis lupus familiaris Yawning Imitation Contagion Empathy Development 



We are grateful to all the dogs and owners that participated in the study and thank Ramiro Joly-Mascheroni, Jordan Zlatev and two anonymous reviewers for ideas and comments on the manuscript. Experimental procedures complied with the Animal Behavior Society Guidelines for the Use of Animals in Research. The research was financially supported by the Centre for Cognitive Semiotics (CCS), Lund University and Elisabeth Rausings Minnesfond. Intellectually, the study has benefited from collaboration with the project “Precursors of Sign Use in Intersubjectivity and Imitation” (PSUII), Swedish Research Council.

Supplementary material

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Supplementary material 1 (DOCX 70 kb)


  1. Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10(1):17–21PubMedCrossRefGoogle Scholar
  2. Anderson JR, Matsuzawa T (2006) Yawning: An opening into empathy? In: Matsuzawa T, Tomonaga M, Tanaka M (eds) Cognitive development in chimpanzees. Springer, Heidelberg, pp 233–245CrossRefGoogle Scholar
  3. Anderson JR, Meno P (2003) Psychological influences on yawning in children. Curr Psychol Lett 11(2):1–7Google Scholar
  4. Anderson JR, Myowa-Yamakoshi M, Matsuzawa T (2004) Contagious yawning in chimpanzees. Proc R Soc Lond B 271:S468–S470CrossRefGoogle Scholar
  5. Arnott SR, Singhal A, Goodale MA (2009) An investigation of auditory contagious yawning. Cogn Affec Behav Neurosci 9(3):335–342CrossRefGoogle Scholar
  6. Baron-Cohen S, Wheelwright S (2004) The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Aut Dev Disord 34(2):163–175CrossRefGoogle Scholar
  7. Beerda B, Schilder MBH, van Hooff JARAM, de Vries HW, Mol JA (1998) Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Appl Anim Behav Sci 58:365–381CrossRefGoogle Scholar
  8. Campbell MW, de Waal FBM (2010) Methodological problems in the study of contagious yawning. Front Neurol Neurosci 28:120–127PubMedCrossRefGoogle Scholar
  9. Campbell MW, de Waal FBM (2011) Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PLoS One 6(4):e18283PubMedCrossRefGoogle Scholar
  10. Campbell MW, Carter JD, Proctor D, Eisenberg ML, de Waal FB (2009) Computer animations stimulate contagious yawning in chimpanzees. Proc R Soc Lond B 276:4255–4259CrossRefGoogle Scholar
  11. Chartrand TL, Bargh JA (1999) The chameleon effect: the perception-behavior link and social interaction. J Pers Soc Psych 76(6):893–910CrossRefGoogle Scholar
  12. Cooper JJ, Ashton C, Bishop S, West R, Mills DS, Young RJ (2003) Clever hounds: social cognition in the domestic dog (Canis familiaris). Appl Anim Behav Sci 81(3):229–244CrossRefGoogle Scholar
  13. Custance D, Mayer J (2012) Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study. Anim Cogn 15(5):851–859PubMedCrossRefGoogle Scholar
  14. de Waal FBM (2001) The ape and the sushi master. Penguin Books, LondonGoogle Scholar
  15. de Waal FBM (2008) Putting the altruism back into altruism: the evolution of empathy. Ann Rev Psych 59:279–300CrossRefGoogle Scholar
  16. Decety J (2010) The neurodevelopment of empathy in humans. Dev Neurosci 32(4):257–267PubMedCrossRefGoogle Scholar
  17. Deputte BL (1994) Ethological study of yawning in primates. I: quantitative analysis and study of causation in two species of old world monkeys (Cercocebus albigena and Macaca fascicularis). Ethology 98(3–4):221–245Google Scholar
  18. Giganti F, Ziello ME (2009) Contagious and spontaneous yawning in autistic and typically developing children. Curr Psychol Lett 25(1):2–11Google Scholar
  19. Harr AL, Gilbert VR, Phillips KA (2009) Do dogs (Canis familiaris) show contagious yawning? Anim Cogn 12(6):833–837PubMedCrossRefGoogle Scholar
  20. Hatfield E, Rapson RL, Le YL (2009) Emotional contagion and empathy. In: Decety J, Ickes W (eds) The social neuroscience of empathy. MIT Press, Boston, pp 19–30Google Scholar
  21. Helt MS, Eigsti IM, Snyder PJ, Fein DA (2010) Contagious yawning in autistic and typical development. Child Dev 81(5):1620–1631PubMedCrossRefGoogle Scholar
  22. Joly-Mascheroni RM, Senju A, Shepherd AJ (2008) Dogs catch human yawns. Biol Lett 4(5):446–448PubMedCrossRefGoogle Scholar
  23. Jones AC, Josephs RA (2006) Interspecies hormonal interactions between man and the domestic dog (Canis familiaris). Horm Behav 50(3):o393–o400CrossRefGoogle Scholar
  24. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, Chanda ML, Levitin DJ, Mogil JS (2006) Social modulation of pain as evidence for empathy in mice. Science 312(5782):1967–1970PubMedCrossRefGoogle Scholar
  25. Lipps T (1903) Einfühlung, innere Nachahmung und Organempfindung. Arch Ges Psych 1:465–519Google Scholar
  26. Meltzoff AN, Moore MK (1994) Imitation, memory, and the representation of persons. Infant Behav Dev 17(1):83–99CrossRefGoogle Scholar
  27. Miklósi A (2008) Dog behaviour, evolution, and cognition. Oxford University Press, OxfordGoogle Scholar
  28. Millen A, Anderson JR (2011) Neither infants nor toddlers catch yawns from their mothers. Biol Lett 7(3):440–442PubMedCrossRefGoogle Scholar
  29. Miller ML, Gallup AC, Vogel AR, Vicario SM, Clark AB (2011) Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): an observational study of yawning and stretching. Behav Proc 89:264–270CrossRefGoogle Scholar
  30. Niedenthal P, Barsalou LW, Ric F, Krauth-Gruber S (2005) Embodiment in the acquisition and use of emotion knowledge. In: Barrett LF, Niedenthal P, Winkielman P (eds) Emotion and consciousness. Guilford Press, NY, pp 21–50Google Scholar
  31. Norscia I, Palagi E (2011) Yawn contagion and empathy in Homo sapiens. PLoS ONE 6(12):e28472PubMedCrossRefGoogle Scholar
  32. O’Hara SJ, Reeve AV (2010) A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris. Anim Behav 81:335–340CrossRefGoogle Scholar
  33. Palagi E, Leone A, Mancini G, Ferrari PF (2009) Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci 106(46):19262–19267PubMedCrossRefGoogle Scholar
  34. Paukner A, Anderson JR (2006) Video-induced yawning in stumptail macaques (Macaca arctoides). Biol Lett 2(1):36–38PubMedCrossRefGoogle Scholar
  35. Piaget J (1951) Play, dreams, and imitation in childhood. Norton, New YorkGoogle Scholar
  36. Platek SM, Critton SR, Myers TE, Gallup GG (2003) Contagious yawning: the role of self-awareness and mental state attribution. Cogn Brain Res 17(2):223–237CrossRefGoogle Scholar
  37. Povinelli DJ, Rulf AB, Bierschwale DT (1994) Absence of knowledge attribution and self-recognition in young chimpanzees (Pan troglodytes). J Comp Psych 108(1):74–80CrossRefGoogle Scholar
  38. Preston SD, de Waal FBM (2002) Empathy: its ultimate and proximate bases. BBS 25:1–72Google Scholar
  39. Provine RR (1986) Yawning as a stereotyped action pattern and releasing stimulus. Ethology 72:109–122CrossRefGoogle Scholar
  40. Saxe R, Carey S, Kanwisher N (2004) Understanding other minds: linking developmental psychology and functional neuroimaging. Ann Rev Psychol 55:87–124CrossRefGoogle Scholar
  41. Senju A (2010) Developmental and comparative perspectives of contagious yawning. Front Neurol Neurosci 28:113–119PubMedCrossRefGoogle Scholar
  42. Senju A, Maeda M, Kikuchi Y, Hasegawa T, Tojo Y, Osanai H (2007) Absence of contagious yawning in children with autism spectrum disorder. Biol Lett 3(6):706–708PubMedCrossRefGoogle Scholar
  43. Senju A, Kikuchi Y, Akechi H, Hasegawa T, Tojo Y, Osanai H (2009) Brief report: does eye contact induce contagious yawning in children with autism spectrum disorder? J Aut Dev Disord 39(11):1598–1602CrossRefGoogle Scholar
  44. Silva K, Bessa J, de Sousa L (2012) Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation. Anim Cogn 15(4):721–724PubMedCrossRefGoogle Scholar
  45. Singer T (2006) The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neurosci Biobehav Rev 30(6):855–863PubMedCrossRefGoogle Scholar
  46. Topál J, Gácsi M, Miklósi Á, Virányi Z, Kubinyi E, Csányi V (2005) Attachment to humans: a comparative study on hand-reared wolves and differently socialized dog puppies. Anim Behav 70(6):1367–1375CrossRefGoogle Scholar
  47. Walusinski O (2010) The mystery of yawning in physiology and disease. Frontiers of neurology and neuroscience. Karger, BaselGoogle Scholar
  48. Wellman HM, Cross D, Watson J (2001) Meta-analysis of theory-of-mind development: the truth about false belief. Chi Dev 72(3):655–684CrossRefGoogle Scholar
  49. Wiggers M, Van Lieshout CF (1985) Development of recognition of emotions: children’s reliance on situational and facial expressive cues. Dev Psych 21(2):338–349CrossRefGoogle Scholar
  50. Wilkinson A, Sebanz N, Mandl I, Huber L (2011) No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria. Curr Zool 57:477–484Google Scholar
  51. Yoon J, Tennie C (2010) Contagious yawning: a reflection of empathy, mimicry, or contagion? Anim Behav 79:e1–e3CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Centre for Languages and Literature, Department of SemioticsLund UniversityLundSweden
  2. 2.Department of Cognitive ScienceLund UniversityLundSweden

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