Play like me: Similarity in playfulness promotes social play

Autoři: Jessica Frances Lampe aff001;  Sabrina Ruchti aff001;  Oliver Burman aff002;  Hanno Würbel aff001;  Luca Melotti aff001
Působiště autorů: Division of Animal Welfare, University of Bern, Bern, Switzerland aff001;  School of Life Sciences, University of Lincoln, Joseph Banks Laboratories, Lincoln, United Kingdom aff002;  Department of Behavioural Biology, University of Münster, Münster, Germany aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224282


Social play is associated with the experience of positive emotions in higher vertebrates and may be used as a measure of animal welfare. Altering motivation to play (e.g., through short-term social isolation) can temporarily affect play levels between familiar individuals, a process which may involve emotional contagion. This study investigated how forming groups based on known differences in the personality trait “playfulness” (i.e., the longer-term propensity of an individual to actively play from adolescence to early adulthood) affects social play. Seventy-six adolescent male Lister Hooded rats underwent a Play-in-Pairs test assessing their playfulness, ranked as high (H), intermediate (I) or low (L). At seven weeks of age, rats were resorted into homogenous groups of similar (LLL, III, HHH), or heterogeneous groups of dissimilar (HII, LII) playfulness. Social play was scored in the home cage at Weeks 8, 10, 12 of age. A second Play-in-Pairs test was performed (Week 11) to assess consistency of playfulness. A Social Preference test investigated whether I rats in heterogeneous groups preferred proximity with I, H or L cage mates. It was found that heterogeneous groups played less than homogeneous ones at adolescence (8 weeks of age), while play levels at early adulthood (Weeks 10 and 12) did not differ between groups. Play in the homogeneous groups decreased with age as expected, while it did not change over time in the heterogeneous groups, which did not compensate for the lower play levels shown at adolescence. Play-in-Pairs scores before and after resorting were mildly correlated, indicating some level of consistency over time despite the resorting procedure. In the Social Preference test, subjects did not prefer one playfulness level over another. We conclude that a mismatch in playfulness may negatively affect social play development, and thus the welfare, of rats. Groups made of animals with similar playfulness, even those initially scoring relatively low in this trait, seemed to be more successful in establishing play relationships during adolescence.

Klíčová slova:

Animal welfare – Behavior – Emotions – Imitation – Motivation – Personality – Rats – Social play


1. Burghardt G. The genesis of animal play: integrative and comparative biology. ICB. 2005;45:953.

2. Spinka M, Newberry RC, Bekoff M. Mammalian Play: training for the unexpected. Q Rev Biol. 2001;76(2):141–168. 11409050

3. Diamond J, Bond AB. A comparative analysis of social play in birds. Behaviour. 2003;140:1091–1115.

4. Held SDE, Spinka M. Animal play and animal welfare. Anim Behav. 2011; 81:891–899.

5. Panksepp J. The ontogeny of play in rats. Dev Psychobiol. 1981;14: 327–332. doi: 10.1002/dev.420140405 7250521

6. Pellis SM, Pellis VC. Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat rattus norvegicus. Aggr Behav. 1987;13:227–242.

7. Pellis SM, McKenna MM. Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate. Behav Brain Res. 1992;50:135–145. doi: 10.1016/s0166-4328(05)80295-5 1449641

8. Pellis SM, Field EF, Smith LK, Pellis VC. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci Biobehav Rev. 1997;21(1):105–120. 8994213

9. Douglas LA, Varlinskaya EI, Spear LP. Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol. 2004;45:153–162. doi: 10.1002/dev.20025 15505797

10. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol. 2008;122:357–367. doi: 10.1037/a0012889 19014259

11. Knutson B, Burgdorf J, Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull. 2002;128(6):961. doi: 10.1037/0033-2909.128.6.961 12405139

12. Calcagnetti DJ, Schechter MD. Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav. 1992;51:667–672. doi: 10.1016/0031-9384(92)90101-7 1594664

13. Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling, et al. Assessment of positive emotions in animals to improve their welfare. Physiol Behav. 2007;92:375–397. doi: 10.1016/j.physbeh.2007.02.003 17428510

14. Oliveira A, Rossi A, Silva L, Lau M, Barreto R. Play behaviour in nonhuman animals and the animal welfare issue. J Ethol. 2010;28: 1–5.

15. Vanderschuren LJMJ. How the brain makes play fun. Am J Play. 2010; 2:315–337.

16. Vanderschuren LJMJ, Stein EA, Wiegant VM, van Ree JM. Social play alters regional brain opioid receptor binding in juvenile rats. Brain Res. 1995;680:148–156. doi: 10.1016/0006-8993(95)00256-p 7663971

17. Humphreys AP, Einon DF. Play as a reinforcer for maze-learning in juvenile rats. Anim Behav. 1981;29:259–270.

18. Vanderschuren LJMJ, Niesink RJM, van Ree JM. The neurobiology of social play behaviour in rats. Neurosci Biobehav Rev. 1997;21(3):309–326. 9168267

19. Palagi E, Paoli T, Tarli SB. Short-term benefits of play behavior and conflict prevention in Pan paniscus. Int J Primatol. 2006;27(5):1257–70.

20. Antonacci D, Norscia I, Palagi E. Stranger to familiar: wild strepsirhines manage xenophobia by playing. PloS one. 2010;5(10):e13218. doi: 10.1371/journal.pone.0013218 20949052

21. Bateson P, Mendl M, Feaver J. Play in the domestic cat is enhanced by rationing of the mother during lactation. Animal Behav. 1990;40(3):514–25.

22. De Waal FB. Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 2008;59:279–300. doi: 10.1146/annurev.psych.59.103006.093625 17550343

23. Hatfield E., Cacioppo JT, & Rapson RL. Emotional Contagion. New York, NY: Cambridge University Press; 1994.

24. Preston SD, De Waal FB. The communication of emotions and the possibility of empathy in animals. Altruism and altruistic love. 2002;284–308.

25. Ferrari PF, Bonini L, Fogassi L. From monkey mirror neurons to primate behaviours: possible ‘direct’and ‘indirect’pathways. Philos Trans Royal Soc B. 2009;364(1528):2311–23.

26. Špinka M. Social dimension of emotions and its implication for animal welfare. Appl Anim Behav Sci. 2012;138:170–181.

27. Reimert I, Bolhuis JE, Kemp B, & Rodenburg B. Indicators of positive and negative emotions and emotional contagion in pigs. Physiol Behav. 2013;109(1): 42–50.

28. Spoor JR, Kelly JR. The evolutionary significance of affect in groups: Communication and group bonding. Group Process Intergroup Relat. 2004;7(4):398–412.

29. Seyfarth RM, Cheney DL. Affiliation, empathy, and the origins of theory of mind. PNAS. 2013; 110(2):10349–10356.

30. Fischer A, Becker D, Veenstra L. Emotional mimicry in social context: the case of disgust and pride. Front Psychol. 2012; 3:475. doi: 10.3389/fpsyg.2012.00475 23130013

31. Kim EJ, Kim ES, Covey E, Kim JJ. Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PloS one. 2010;5(12):e15077. doi: 10.1371/journal.pone.0015077 21152023

32. Knapska E, Mikosz M, Werka T, Maren S. Social modulation of learning in rats. Learn Mem. 2010;17:824–831.

33. Goumon S, Spinka M. Emotional contagion of distress in young pigs is potentiated by previous exposure to the same stressor. Anim Cog. 2016; 19(3):501–511.

34. Boyko M, Kutz R, Grinshpun J, Zvenigorodsky V, Gruenbaum SE, Gruenbaum BF et al. Establishment of an animal model of depression contagion. Behav Brain Res. 2015;281:358–363. doi: 10.1016/j.bbr.2014.12.017 25523029

35. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS et al. Social modulation of pain as evidence for empathy in mice. Science. 2006; 312(5782):1967–1970. doi: 10.1126/science.1128322 16809545

36. Edgar JL, Nicol CJ, Clark CCA, Paul ES. Measuring empathic responses in animals. Appl Anim Behav Sci. 2012;138(3–4): 82–193.

37. Barsade SG. The ripple effect: emotional contagion and its influence on group behavior. Admin Sci Q. 2002;47(4):644–675.

38. Bono JE, Ilies R. Charisma, positive emotions and mood contagion. Leadership Quart. 2006; 17:317–344

39. Kramer ADI, Guillory JE, Hancock JT. Experimental evidence of massive-scale emotional contagion through social networks. PNAS. 2014;111(24): 8788–8790. doi: 10.1073/pnas.1320040111 24889601

40. Davila Ross M, Menzler S, Zimmermann E. Rapid facial mimicry in orangutan play. Biol Lett. 2008;4(1):27–30. doi: 10.1098/rsbl.2007.0535 18077238

41. Parr LA, Hopkins WD. Brain temperature asymmetries and emotional perception in chimpanzees, Pan troglodytes. Physiol Behav. 2000;71(3–4):363–71. doi: 10.1016/s0031-9384(00)00349-8 11150569

42. Palagi E, Nicotra V, Cordoni G. Rapid mimicry and emotional contagion in domestic dogs. Royal Soc Open Sci. 2015;2(12):150505.

43. Huber A, Barber AL, Faragó T, Müller CA, Huber L. Investigating emotional contagion in dogs (Canis familiaris) to emotional sounds of humans and conspecifics. Anim Cogn. 2017;20(4):703–15. doi: 10.1007/s10071-017-1092-8 28432495

44. Varlinskaya EI, Spear LP, Spear NE. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiol Behav. 1999;67:475–482. doi: 10.1016/s0031-9384(98)00285-6 10549884

45. Lampe JF, Burman O, Würbel H, Melotti L. Context-dependent individual differences in playfulness in male rats. Dev Psychobiol. 2017;59(4):460–472. doi: 10.1002/dev.21509 28247407

46. Melotti L, Bailoo JD, Murphy E, Burman OHP, Würbel H. Play in rats: association across contexts and types, and analysis of structure. Anim Behav Cogn. 2014;1(4):489–501.

47. Poole TB, Fish J. An investigation of individual, age and sexual differences in the play of rattus norvegicus (mammalia: rodentia). J Zool Lond. 1976;179:249–260.

48. Dewsbury DA. Tests of preferences of young deer mice (Peromyscus maniculatus bairdi) for siblings versus nonsiblings. J Comp Psychol. 1990;104(2):174–176. 2364662

49. Finlayson K, Lampe JF, Hintze S, Würbel H, Melotti L. Facial indicators of positive emotions in rats. PLoS one. 2016;11(11):e0166446. doi: 10.1371/journal.pone.0166446 27902721

50. Vanderschuren LJMJ, Niesink RJM, Spruijt BM, van Ree JM. Influence of environmental factors on social play behavior of juvenile rats. Physiol Behav. 1995;58:119–123. doi: 10.1016/0031-9384(94)00385-i 7667408

51. Niesink RJM, van Ree J. Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacol. 1989;28:411–18.

52. Panksepp J, Beatty WW. Social deprivation and play in rats. Behav Neural Biol. 1980;30:197–206. doi: 10.1016/s0163-1047(80)91077-8 7447871

53. Hurst JL, Barnard CJ, Hare R, Wheeldon EB, West CD. Housing and welfare in laboratory rats: time-budgeting and pathophysiology in single-sex groups. Anim Behav. 1996;52(2):335–360.

54. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A, et al. Automated apparatus for quantification of social approach behaviours in mice. Genes Brain Behav. 2004;3:303–314. doi: 10.1111/j.1601-183X.2004.00071.x 15344923

55. Enders CK, Tofighi D. Centering predictor variables in cross-sectional multilevel models: A new look at an old issue. Psychol Methods. 2007; 12(2):121–138. doi: 10.1037/1082-989X.12.2.121 17563168

56. Pellis S, Pellis V. Rough-and-tumble play and the development of the social brain. Cur Dir Psychol. 2007;16(2):95–98.

57. Izard C. Personality similarity and friendship. J Abnorm Soc Psychol. 1960; 61(1):47–51.

58. Perrone KM, Sedlacek WE. A comparison of group cohesiveness and client satisfaction in homogenous and heterogenous groups. J Spec Group Work. 2000;25(3):243–251.

59. McPherson M, Smith-Lovin L, Cook JM. Birds of a feather: homophily in social networks. Annu Rev of Sociol. 2001;27:415–444.

60. Selfhout M, Burk W, Branje S, Denissen J, Van Akten M, Meeus W. Emerging late adolescent friendship networks and big five personality traits: a social network approach. J Personal. 2010;78(2):509–538.

61. Massen JJM, Koski SE. Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav. 2014;35:1–8.

62. Briard L, Dorn C, Petit O. Personality and affinities play a key role in the organisation of collective movements in a group of domestic horses. Ethology. 2015;121(9):888–902.

63. Turcsán B, Range F, Virányi Z, Miklósi Á, Kubinyi E. Birds of a feather flock together? Perceived personality matching in owner-dog dyads. Appl Anim Behav Sci. 2012;140(3–4):154–160.

64. Pellis SM, Hastings E, Shimizu T, Kamitakahara H, Komorowska J, Forgie ML, et al. The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and non-playful social contexts. Behav Neurosci. 2006;120:72–84. doi: 10.1037/0735-7044.120.1.72 16492118

65. Himmler SM., Himmler BT., Stryjek R., Modlińska K., Pisula W., & Pellis SM. Pinning in the play fighting of rats: A comparative perspective with some methodological recommendations. Int J Comp Psychol. 2016; 29:1–14.

66. Reinhart CJ, Pellis SM, McIntyre DC. Development of play fighting in kindling‐prone (FAST) and kindling‐resistant (SLOW) rats: How does the retention of phenotypic juvenility affect the complexity of play? Dev Psychobiol. 2004;45(2):83–92. doi: 10.1002/dev.20016 15340977

67. Specht J, Egloff B, Schmukle SC. Stability and change of personality across the life course: The impact of age and major life events on mean-level and rank-order stability of the Big Five. J Pers Soc Psychol. 2011;101:862–882. doi: 10.1037/a0024950 21859226

68. Pellis SM, Pellis VC. Role reversal changes during the ontogeny of play fighting in male rats: Attack vs. defense. Aggres Behav. 1991;17(3):179–89.

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