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

Abstract

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.

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

Fig. 1

Notes

  1. 1.

    Tension yawns and ‘sleepy’ yawns are morphologically identical, only distinguished by the context and the co-occurrence of either, none or all of a number of associated behaviours, e.g. lip licking, scratching, body shaking (‘shaking it off’), panting, whimpering or sneezing.

  2. 2.

    Analysis was based on 64 (rather than 70) trials, as the number of gapes could not be reliably coded in six trials (as the experimenter at times faced away from the camcorders).

References

  1. Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10(1):17–21

    PubMed  Article  Google 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 233–245

    Google Scholar 

  3. Anderson JR, Meno P (2003) Psychological influences on yawning in children. Curr Psychol Lett 11(2):1–7

    Google Scholar 

  4. Anderson JR, Myowa-Yamakoshi M, Matsuzawa T (2004) Contagious yawning in chimpanzees. Proc R Soc Lond B 271:S468–S470

    Article  Google Scholar 

  5. Arnott SR, Singhal A, Goodale MA (2009) An investigation of auditory contagious yawning. Cogn Affec Behav Neurosci 9(3):335–342

    Article  Google 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):163–175

    Article  Google 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 58:365–381

    Article  Google Scholar 

  8. Campbell MW, de Waal FBM (2010) Methodological problems in the study of contagious yawning. Front Neurol Neurosci 28:120–127

    PubMed  Article  Google Scholar 

  9. Campbell MW, de Waal FBM (2011) Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PLoS One 6(4):e18283

    PubMed  Article  CAS  Google 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 276:4255–4259

    Article  Google Scholar 

  11. Chartrand TL, Bargh JA (1999) The chameleon effect: the perception-behavior link and social interaction. J Pers Soc Psych 76(6):893–910

    Article  CAS  Google 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):229–244

    Article  Google 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):851–859

    PubMed  Article  Google Scholar 

  14. de Waal FBM (2001) The ape and the sushi master. Penguin Books, London

    Google Scholar 

  15. de Waal FBM (2008) Putting the altruism back into altruism: the evolution of empathy. Ann Rev Psych 59:279–300

    Article  Google Scholar 

  16. Decety J (2010) The neurodevelopment of empathy in humans. Dev Neurosci 32(4):257–267

    PubMed  Article  CAS  Google 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):221–245

    Google Scholar 

  18. Giganti F, Ziello ME (2009) Contagious and spontaneous yawning in autistic and typically developing children. Curr Psychol Lett 25(1):2–11

    Google Scholar 

  19. Harr AL, Gilbert VR, Phillips KA (2009) Do dogs (Canis familiaris) show contagious yawning? Anim Cogn 12(6):833–837

    PubMed  Article  Google 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 19–30

    Google Scholar 

  21. Helt MS, Eigsti IM, Snyder PJ, Fein DA (2010) Contagious yawning in autistic and typical development. Child Dev 81(5):1620–1631

    PubMed  Article  Google Scholar 

  22. Joly-Mascheroni RM, Senju A, Shepherd AJ (2008) Dogs catch human yawns. Biol Lett 4(5):446–448

    PubMed  Article  Google Scholar 

  23. Jones AC, Josephs RA (2006) Interspecies hormonal interactions between man and the domestic dog (Canis familiaris). Horm Behav 50(3):o393–o400

    Article  Google 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):1967–1970

    PubMed  Article  CAS  Google Scholar 

  25. Lipps T (1903) Einfühlung, innere Nachahmung und Organempfindung. Arch Ges Psych 1:465–519

    Google Scholar 

  26. Meltzoff AN, Moore MK (1994) Imitation, memory, and the representation of persons. Infant Behav Dev 17(1):83–99

    Article  Google Scholar 

  27. Miklósi A (2008) Dog behaviour, evolution, and cognition. Oxford University Press, Oxford

    Google Scholar 

  28. Millen A, Anderson JR (2011) Neither infants nor toddlers catch yawns from their mothers. Biol Lett 7(3):440–442

    PubMed  Article  Google 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 89:264–270

    Article  Google 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 21–50

    Google Scholar 

  31. Norscia I, Palagi E (2011) Yawn contagion and empathy in Homo sapiens. PLoS ONE 6(12):e28472

    PubMed  Article  CAS  Google Scholar 

  32. O’Hara SJ, Reeve AV (2010) A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris. Anim Behav 81:335–340

    Article  Google 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):19262–19267

    PubMed  Article  CAS  Google Scholar 

  34. Paukner A, Anderson JR (2006) Video-induced yawning in stumptail macaques (Macaca arctoides). Biol Lett 2(1):36–38

    PubMed  Article  Google Scholar 

  35. Piaget J (1951) Play, dreams, and imitation in childhood. Norton, New York

    Google 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):223–237

    Article  Google 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):74–80

    Article  CAS  Google Scholar 

  38. Preston SD, de Waal FBM (2002) Empathy: its ultimate and proximate bases. BBS 25:1–72

    Google Scholar 

  39. Provine RR (1986) Yawning as a stereotyped action pattern and releasing stimulus. Ethology 72:109–122

    Article  Google Scholar 

  40. Saxe R, Carey S, Kanwisher N (2004) Understanding other minds: linking developmental psychology and functional neuroimaging. Ann Rev Psychol 55:87–124

    Article  CAS  Google Scholar 

  41. Senju A (2010) Developmental and comparative perspectives of contagious yawning. Front Neurol Neurosci 28:113–119

    PubMed  Article  Google 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):706–708

    PubMed  Article  Google 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):1598–1602

    Article  Google 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):721–724

    PubMed  Article  Google 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):855–863

    PubMed  Article  Google 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):1367–1375

    Article  Google Scholar 

  47. Walusinski O (2010) The mystery of yawning in physiology and disease. Frontiers of neurology and neuroscience. Karger, Basel

  48. Wellman HM, Cross D, Watson J (2001) Meta-analysis of theory-of-mind development: the truth about false belief. Chi Dev 72(3):655–684

    Article  CAS  Google 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):338–349

    Article  Google 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 57:477–484

    Google Scholar 

  51. Yoon J, Tennie C (2010) Contagious yawning: a reflection of empathy, mimicry, or contagion? Anim Behav 79:e1–e3

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Elainie Alenkær Madsen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 70 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Madsen, E.A., Persson, T. Contagious yawning in domestic dog puppies (Canis lupus familiaris): the effect of ontogeny and emotional closeness on low-level imitation in dogs. Anim Cogn 16, 233–240 (2013). https://doi.org/10.1007/s10071-012-0568-9

Download citation

Keywords

  • Canis lupus familiaris
  • Yawning
  • Imitation
  • Contagion
  • Empathy
  • Development