Abstract
Domestic dogs are a highly playful species that are evidently sensitive to the attentional state of conspecifics as well as humans. Given that an animal’s social environment can influence play, audience effects may catalyze social play. While prior research has shown that intraspecific attention maintains social play in dog–dog dyads, it is unknown whether interspecific (specifically, human) attention maintains social play between dogs. Our objective in the present study was to examine whether a relationship exists between the availability of human attention and social play in domestic dogs. Familiar dog–dog dyads were exposed to three sessions each consisting of three experimental conditions that differed in the degree of availability of owner attention. Observed levels of social play were significantly higher during conditions in which an attentive owner was present than during conditions in which an owner was either inattentive or absent. Furthermore, this effect was maintained across repeated sessions. This is the first experimental evidence of an interspecific audience effect facilitating social play in domestic dogs. The availability of caretaker attention may be a proximate explanation for social play in canids that have ontogenetically rich histories with humans and also retain neotonized behavior as adults. Further research is needed to clarify the mechanisms contributing to the relationship between interspecific attention and social play in these populations and establish a more comprehensive understanding of play behavior in animals.
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The data used for this study are available from the corresponding author on request.
References
Baldwin JD, Baldwin JI (1973) The role of play in social organization: Comparative observations on squirrel monkeys (Saimiri). Primates 14(4):369–381. https://doi.org/10.1007/BF01731358
Bates D, Mächler M, Bolker B, Walker S (2015) “Fitting Linear Mixed-Effects Models Using lme4.” J Statist Software 67(1): 1–48. https://doi.org/10.18637/jss.v067.i01
Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs Canis familiaris. Animal Behav 73(3):489–499. https://doi.org/10.1016/j.anbehav.2006.09.006
Bekoff M (1977) Mammalian dispersal and the ontogeny of individual behavioral phenotypes. Am Nat 111:715–732. https://doi.org/10.1086/283201
Bekoff M (1984) Social play behavior. Bioscience 34:228–233. https://doi.org/10.2307/1309460
Bekoff M (1995) Play signals as punctuation: the structure of social play in canids. Behaviour 132:419–429. https://doi.org/10.1163/156853995X00649
Bekoff M (2001) Social play behaviour. Cooperation, fairness, trust, and the evolution of morality. J Consciousness Stud 8(2):81–90
Bekoff M, Byers JA (1981) A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: an ethological hornet’s nest. In: Immelmann BGW, Petrinovich Lain M (eds) Behavioral Development. Cambridge Univ. Press, London
Bekoff M, Byers J (1998) Animal play: Evolutionary, comparative, and ecological perspectives. Cambridge University Press, Cambridge
Berger J (1980) The ecology, structure and functions of social play in bighorn sheep (Ovis canadensis). J Zool 192(4):531–542. https://doi.org/10.1111/j.1469-7998.1980.tb04248.x
Blumstein DT, Wey TW, Tang K (2009) A test of the social cohesion hypothesis: interactive female marmots remain at home. Proc Royal Soc B Biol Sci 276(1669):3007–3012
Brucks D, Essler JL, Marshall-Pescini S, Range F (2016) Inequity aversion negatively affects tolerance and contact-seeking behaviors towards partner and experimenter. PLoS ONE 11(4):e0153799. https://doi.org/10.1371/journal.pone.0153799
Brueggeman JA (1978) The function of adult play in free-living Macaca mulatta. In: Smith EO (ed) Social play in primates. Academic Press, New York, pp 169–192
Burghardt GM (2005) The genesis of animal play. Cambridge University Press, Cambridge
Burghardt GM (2010) The comparative reach of play and brain: Perspective, evidence, and implications. Am J Play 2(3):338–356
Burkart JM, van Schaik CP (2020) Marmoset prosociality is intentional. Anim Cogn. https://doi.org/10.1007/s10071-020-01363-6
Cools AK, Van Hout AJM, Nelissen MH (2008) Canine reconciliation and third-party-initiated postconflict affiliation: do peacemaking social mechanisms in dogs rival those of higher primates? Ethology 114(1):53–63. https://doi.org/10.1111/j.1439-0310.2007.01443.x
Coppinger B, Cannistraci RA, Karaman F, Kyle SC, Hobson EA, Freeberg TM, Hay JF (2017) Studying audience effects in animals what we can learn from human language research. Animal Behav 124:161–165. https://doi.org/10.1016/j.anbehav.2016.12.020
Coppinger BA, Kania SA, Lucas JR, Sieving KE, Freeberg TM (2020) Experimental manipulation of mixed-species flocks reveals heterospecific audience effects on calling. Anim Behav 167:193–207
Cordoni G (2009) Social play in captive wolves (Canis lupus): Not only an immature affair. Behaviour 146:1363–1385. https://doi.org/10.1163/156853909X427722
Dillon L (2013) Functional aspects of jealousy across the lifespan. Human Ethol Bull 28(2):13–26
Dorey NR, Tobias JS, Udell MAR, Wynne CDL (2012) Decreasing dog problem behavior with functional analysis: Linking diagnoses to treatment. J Vet Behav 7(5):276–282
Dzieweczynski TL, Earley RL, Green TM, Rowland WJ (2005) Audience effect is context dependent in Siamese fighting fish. Betta splendens Behav Ecol 16(6):1025–1030. https://doi.org/10.1093/beheco/ari088
Essler JL, Marshall-Pescini S, Range F (2017) Domestication does not explain the presence of inequity aversion in dogs. Curr Biol 27(12):1861–1865. https://doi.org/10.1016/j.cub.2017.05.061
Fagen R (1981) Animal Play Behavior. Oxford University Press, New York
Feuerbacher EN, Wynne CDL (2015) Shut up and pet me! Domestic dogs (Canis lupus familiaris) prefer petting to vocal praise in concurrent and single-alternative choice procedures. Behav Processes 110:47–59. https://doi.org/10.1016/j.beproc.2014.08.019
Hall S (1998) Object play by adult animals. In: Bekoff M, Byers J (eds) Animal play: Evolutionary, comparative, and ecological perspectives. Cambridge University Press, Cambridge
Hall S, Bradshaw JWS (1998) The influence of hunger on object play by adult domestic cats. Appl Animal Behav Sci 58:143–150. https://doi.org/10.1016/S0168-1591(97)00136-6
Hall NJ, Protopopova A, Wynne CDL (2015) The role of environmental and owner-provided consequences in canine stereotypy and compulsive behavior. J Vet Behav 10(1):24–35. https://doi.org/10.1016/j.jveb.2014.10.005
Harcourt R (1991) Survivorship costs of play in the South American fur seal. Anim Behav 42:509–511. https://doi.org/10.1016/S0003-3472(05)80055-7
Held SDE, Spinka M (2011) Animal play and animal welfare. Anim Behav 81:891–899. https://doi.org/10.1016/j.anbehav.2011.01.007
Hinde RA (1974) Biological basis of human social behavior. McGraw-Hill, New York
Horowitz A (2012) Fair is fine, but more is better: Limits to inequity aversion in the domestic dog. Soc Justice Res 25(2):195–212
Horowitz CA (2009) Attention to attention in domestic dog (Canis familiaris) dyadic play. Anim Cogn 12:7–18. https://doi.org/10.1007/s10071-008-0175-y
Horowitz A, Hecht J (2016) Examining dog–human play: the characteristics, affect, and vocalizations of a unique interspecific interaction. Anim Cogn 19(4):779–788. https://doi.org/10.1007/s10071-016-0976-3
Iwata BA, Dorsey MF, Slifer KL, Bauman KE, Richman GS (1982/1994) Toward a functional analysis of self-injury. J Appl Behav Analysis 27: 197–209 https://doi.org/10.1016/0270-4684(82)90003-9
Jones SS, Collins K, Hong HW (1991) An audience effect on smile production in 10-month-old infants. Psychol Sci 2(1): 45–49. 10.1111%2Fj.1467-9280.1991.tb00095.x
Kaminski J, Nitzschner M (2013) Do dogs get the point? A review of dog–human communication ability. Learn Motiv 44(4):294–302. https://doi.org/10.1016/j.lmot.2013.05.001
Kaminski J, Hynds J, Morris P, Waller BM (2017) Human attention affects facial expressions in domestic dogs. Scient Rep 7(1):1–7. https://doi.org/10.1038/s41598-017-12781-x
Kobelt AJ, Hemsworth PH, Barnett JL, Coleman GJ, Butler KL (2007) The behaviour of Labrador retrievers in suburban backyards: The relationships between the backyard environment and dog behaviour. Appl Anim Behav Sci 106(1–3):70–84
Koda N (2001) Development of play behavior between potential guide dogs for the blind and human raisers. Behav Proc 53(1–2):41–46. https://doi.org/10.1016/S0376-6357(00)00146-7
Lakatos G, Soproni K, Doka A, Miklósi A (2009) A comparative approach to dogs’ and human infants’ comprehension of various forms of pointing gestures. Anim Cogn 12:621–631. https://doi.org/10.1007/s10071-009-0221-4
Marshall-Pescini S, Colombo E, Passalacqua C, Merola I, Prato-Previde E (2013) Gaze alternation in dogs and toddlers in an unsolvable task: evidence of an audience effect. Anim Cogn 16(6):933–943. https://doi.org/10.1007/s10071-013-0627-x
Martin P, Caro TM (1985) On the functions of play and its role in behavioral development. Adv Study Behav 15:9–103. https://doi.org/10.1016/S0065-3454(08)60487-8
Mehrkam LR, Verdi NL, Wynne CDL (2014) Human interaction as environmental enrichment for pair-housed wolves and wolf-dog crosses. J Appl Anim Welfare Sci 17(1):43–58. https://doi.org/10.1080/10888705.2014.856246
Mehrkam LR, Perez BC, Self VN, Vollmer TR, Dorey NR (2020) Functional analysis and operant treatment of food guarding in a pet dog. J Appl Behav Anal 53(4):2139–2150. https://doi.org/10.1002/jaba.720
Morris PH, Doe C, Godsell E (2008) Secondary emotions in non-primate species? Behavioral reports and subjective claims by animal owners. Cogn Emot 22(1):3–20. https://doi.org/10.1080/02699930701273716
Nawroth C, Brett JM, McElligott AG (2016) Goats display audience-dependent human-directed gazing behavior in a problem-solving task. Biol Let 12(7):20160283. https://doi.org/10.1098/rsbl.2016.0283
Pal SK (2010) Play behavior during early ontogeny in free-ranging dogs (Canis familiaris). Appl Animal Behav Sci 126:140–153. https://doi.org/10.1016/j.applanim.2010.06.005
Palagi E (2007) Play at work: revisiting data focusing on chimpanzees (Pan troglodytes). J Anthropol Sci 85:63–81
Palagi E, Cordoni G, Borgognini Tarli S (2004) Immediate and delayed benefits of play behavior: new evidence from chimpanzees (Pan troglodytes). Ethology 110:949–962. https://doi.org/10.1111/j.1439-0310.2004.01035.x
Palagi E, Tommaso Paoli T, Borgognini Tarli S (2006) Short-term benefits of play behavior and conflict prevention in Pan paniscus. Int J Primatol 27:1257–1270. https://doi.org/10.1111/j.1439-0310.2004.01035.x
Panksepp J (2010) The evolutionary sources of jealousy: Cross-species approaches to fundamental issues. In Hart SL, Legerstee M (Eds.), Handbook of jealousy: Theory, research, and multidisciplinary approaches (p. 101–120). Wiley, Blackwell. https://doi.org/10.1002/9781444323542.ch6
Pellis SM, Iwaniuk AN (2004) Evolving a playful brain: a levels of control approach. Int J Compar Psychol 17:92–118
Pellis SM, Pellis VC (1996) On knowing it’s only play: the role of play signals in play fighting. Aggres Violent Behav 1(3):249–268. https://doi.org/10.1016/1359-1789(95)00016-X
Poirier FE, Bellisari A, Hainesh L (1978) Functions of primate play behavior. In: Smith EO (ed) Social play in primates. Academic Press, London, UK, pp 143–168
Pozis-Francois O, Zahavi A, Zahavi A (2004) Social play in Arabian babblers. Behavior 141:425–450. https://doi.org/10.1163/156853904323066720
Prato-Previde E, Valsecchi P (2014) The immaterial cord: The dog–human attachment bond. In The social dog (pp. 165–189). Academic Press
Prato-Previde E, Nicotra V, Poli SF, Pelosi A, Valsecchi P (2018) Do dogs exhibit jealous behaviors when their owner attends to their companion dog? Animal Cogn 21:703–713. https://doi.org/10.1007/s10071-018-1204-0
Quervel-Chaumette M, Faerber V, Faragó T, Marshall-Pescini S, Range F (2016) Investigating empathy-like responding to conspecifics’ distress in pet dogs. PLoS ONE 11(4):e0152920. https://doi.org/10.1371/journal.pone.0152920
Range F, Horn L, Viranyi Z, Huber L (2009) The absence of reward induces inequity aversion in dogs. Proc Natl Acad Sci 106(1):340–345. https://doi.org/10.1073/pnas.0810957105
Rooney NJ, Bradshaw JW (2002) An experimental study of the effects of play upon the dog–human relationship. Appl Animal Behav Sci 75(2):161–176. https://doi.org/10.1016/S0168-1591(01)00192-7
Rooney NJ, Bradshaw JW (2003) Links between play and dominance and attachment dimensions of dog-human relationships. J Appl Anim Welfare Sci 6(2):67–94. https://doi.org/10.1207/s15327604jaws0602_01
Rooney NJ, Bradshaw JW, Robinson IH (2000) A comparison of dog–dog and dog–human play behavior. Appl Animal Behav Sci 66(3):235–248. https://doi.org/10.1016/S0168-1591(99)00078-7
Rooney NJ, Bradshaw JW, Robinson IH (2001) Do dogs respond to play signals given by humans? Anim Behav 61:715–722. https://doi.org/10.1006/anbe.2000.1661
Rossi AP, Maia CM (2020) Owners frequently report that they reward behaviors of dogs by petting and praising, especially when dogs respond correctly to commands and play with their toys. J Appl Anim Welfare Sci. https://doi.org/10.1080/10888705.2019.1709067
Russell ES (1936) Playing with a dog. Quarterly Rev Biol 11:1–15
Seagraves KM, Arthur BJ, Egnor SR (2016) Evidence for an audience effect in mice: Male social partners alter the male vocal response to female cues. J Exp Biol 219(10):1437–1448. https://doi.org/10.1242/jeb.129361
Shimada M, Sueur C (2018) Social play among juvenile wild Japanese macaques (Macaca fuscata) strengthens their social bonds. Am J Primatol 80(1):e22728. https://doi.org/10.1002/ajp.22728
Smith PK (1982) Does play matter? Functional and evolutionary aspects of animal and human play. Behav Brain Scis 5:139–184. https://doi.org/10.1017/S0140525X0001092
Smith LK, Fantella SLN, Pellis SM (1999) Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent. Aggress Behav 25:141–152. https://doi.org/10.1002/(SICI)1098-2337(1999)25:2%3C141::AID-AB6%3E3.0.CO;2-S
Spinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76(2):141–168. https://doi.org/10.1086/393866
Thompson KV (1998) Self-assessment in juvenile play. In: Bekoff M, Byers JA (eds.), Animal Play: Evolutionary, Comparative, and Ecological Perspectives, Cambridge University Press, Cambridge, UK (1998), pp. 183–204
Tinbergen N (1963) On aims and methods of ethology. Zeitschrift fur Tierpsychologie 20:410–433. https://doi.org/10.1111/j.1439-0310.1963.tb01161.x
Tóth L, Gácsi M, Topál J, Miklósi Á (2008) Playing styles and possible causative factors in dogs’ behavior when playing with humans. Appl Animal Behav Sci 114:473–484. https://doi.org/10.1016/j.applanim.2008.02.011
Udell MAR, Dorey NR, Wynne CDL (2008) Wolves outperform dogs in following human social cues. Anim Behav 76:1767–1773. https://doi.org/10.1016/j.anbehav.2008.07.028
Udell MAR, Spencer JM, Dorey NR, Wynne CD (2012) Human-socialized wolves follow diverse human gestures… and they may not be alone. Int J Compar Psychol 25(2):97–117
Udell MAR, Lord K, Feuerbacher EN, Wynne CDL (2014) A dog’s-eye view of canine cognition. In: Horowitz A (ed.), domestic dog cognition and behavior (pp. 221–240). Springer, Berlin Heidelberg. http://link.springer.com/chapter/https://doi.org/10.1007/978-3-642-53994-7_10
Ward C, Bauer EB, Smuts BB (2008) Partner preferences and asymmetries in social play among domestic dog, Canis lupus familiaris, littermates. Anim Behav 76(4):1187–1199. https://doi.org/10.1016/j.anbehav.2008.06.004
Ward C, Trisko R, Smuts BB (2009) Third-party interventions in dyadic play between littermates of domestic dogs, Canis lupus familiaris. Anim Behav 78:1153–1160. https://doi.org/10.1016/j.anbehav.2009.07.033
Wheat CH, Fitzpatrick J, Tapper I, Temrin H (2018) Wolf (Canis lupus) hybrids highlight the importance of human-directed play behavior during domestication of dogs (Canis familiaris). J Comp Psychol 132(4):373–381. https://doi.org/10.1037/com0000119
Zahavi A (1977) The testing of a bond. Anim Behav 25:246–247. https://doi.org/10.1016/0003-3472(77)90089-6
Acknowledgements
We would like to thank Dr. David Darmon for his expert and generous help with the statistical analyses for the present study. We would also like to acknowledge Lindsey Wellmaker and Ashley LiCausi for assistance with data coding, as well as three anonymous reviewers for their constructive feedback on an earlier version of this manuscript. Finally, we are grateful to the owners who volunteered their dogs for this study and thank them for their role in making this study possible.
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Mehrkam, L.R., Wynne, C.D.L. Owner attention facilitates social play in dog–dog dyads (Canis lupus familiaris): evidence for an interspecific audience effect. Anim Cogn 24, 341–352 (2021). https://doi.org/10.1007/s10071-021-01481-9
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DOI: https://doi.org/10.1007/s10071-021-01481-9