Social play changes reflect differences in biology and development of three felids

Social play changes reflect differences in biology and development of three felids

Antonevich A.L., Alekseeva G.S., Vasilieva N.A., Pavlova E.V., Loshchagina J.A., Duplyakina S.Yu., Naidenko S.V.

P. 80-90

Social play in young mammals reflects behavioral development, play can be affected by differences in development timing and species biology. We compared social play frequency changes in three felids: Eurasian lynx (Lynx lynx), Amur subspecies of leopard cat (Far-Eastern wildcat) (Prionailurus bengalensis euptilurus) and domestic cat (Felis catus). Social play is often expected to increase social tolerance and cohesion in a litter. Socially living domestic cat had contact and non-contact social play rates at the same level as solitary lynx and leopard cat. Whereas lynx differed from the other felids in lower social play rates at the age from one to one and a half month. Two types of social play were changing differently. Non-contact play rates, attributed to predatory skills development, were synchronized among species by age of kittens. Whereas contact play changes, attributed to communication development, were sensitive to the developmental stage. Contact play intensified in lynx much later than in the other felids probably due to a later onset of weaning. The period of extraordinary low contact play rates coincided with the onset of spontaneous sibling aggression, unique for lynx. After a period of spontaneous sibling aggression contact play rates in lynx increased to the level that other felids had. Observed social play changes and differences reflect development timing and species-specific features in felids.DOI: 10.15298/rusjtheriol.18.2.02

Литература
  • Alekseeva G.S., Antonevich A.L., Erofeeva M.N. & Naidenko S.V. 2014. Social play in the development of sibling relations in Eurasian lynx (Lynx lynx) // Biology Bulletin. Vol.41. No.4. P.364–371.
  • Antonevich A.L. & Naidenko S.V. 2007. [Early sibling aggression in mammals and its hormonal correlates] // Zhurnal Obshchei Biologii. Vol.68. No.4. P.307–317 [in Russian, with English summary].
  • Antonevich A.L. & Naidenko S.V. 2008. Effect of sibling aggression on kittens’ behavior in Eurasian lynx Lynx lynx // Acta Zoologica Sinica. Vol.54. No.11. P.12–19.
  • Antonevich A.L. & Naidenko S.V. 2013. A third species of lynx, the bobcat, was found to experience early sibling aggression // CAT News. Vol.59. P.31–32.
  • Antonevich A.L., Naidenko S.V., Bergara J., Vasques E., Vasques A., Lopez J., Pardo A., Rivas A., Chaparro J.M., Martinez F. & Vargas A. 2009. A comparative note on early sibling aggression in two related species: the Iberian and the Eurasian Lynx // Vargas A. (ed.) Iberian lynx ex-situ conservation: An Interdisciplinary approach. Madrid: Fundación Biodiversidad. P.156–163.
  • Auger A.P. & Olesen K.M. 2009. Brain sex differences and the organisation of juvenile social play behaviour // Journal of Neuroendocrinology. Vol.21. No.6. P.519–525.
  • Ballerini M., Cabibbo N., Candelier R., Cavagna A., Cisbani E., Giardina I., Lecomte V., Orlandi A., Parisi G., Procaccini A., Viale M. & Zdravkovic V. 2008. Interaction ruling animal collective behavior depends on topological rather than metric distance: Evidence from a field study // Proceedings of the National Academy of Sciences of the USA. Vol.105. No.4. P.1232–1237.
  • Barrett P.& Bateson P. 1978. The development of play in cats // Behaviour. Vol.66. No.1. P.106–120.
  • Bartoń K. 2018. MuMIn: Multi-model inference (Version 1.42. 1).
  • Bates D., Mächler M., Bolker B. & Walker S. 2015. Fitting linear mixed-effects models using lme4 // Journal of Statistical Software. Vol.67. No.1. P.1–48.
  • Bateson P.2000. Behavioural development in the cat // Turner D.C., Bateson P.(eds.) The domestic cat: the biology of its behaviour. Cambridge: Cambridge University Press. P.9–23.
  • Bateson P., Mendl M. & Feaver J. 1990. Play in the domestic cat is enhanced by rationing of the mother during lactation // Animal Behaviour. Vol.40. No.3. P.514–525.
  • Bateson P.& Young M. 1981. Separation from the mother and the development of play in cats // Animal Behaviour. Vol.29. No.1. P.173–180.
  • Bekoff M. 1972. The development of social interaction, play, and metacommunication in ammals: An ethological perspective // Quarterly Review of Biology. Vol.47. No.4. P.412–434.
  • Bekoff M. 1974. Social play and play-soliciting by infant canids // American Zoologist. Vol.14. No.1. P.323–340.
  • Biben M. 1983. Comparative ontogeny of social behaviour in three South American canids, the maned wolf, crab-eating fox and bush dog: Implications for sociality // Animal Behaviour. Vol.31. No.3. P.814–826.
  • Blumstein D.T., Chung L.K. & Smith J.E. 2013. Early play may predict later dominance relationships in yellow-bellied marmots (Marmota flaviventris) // Proceedings of the Royal Society of London, B: Biological Sciences. Vol.280. No.1759. 20130485.
  • Brownlee A. 1954. Play in domestic cattle in Britain: an analysis of its nature // British Veterinary Journal. Vol.110. No.2. P.48–69.
  • Burghardt G.M. 2005. The genesis of animal play. Testing the limits. Cambridge: The MIT Press. 520 p.
  • Burnham K.P. & Anderson D.R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer Science & Business Media. 488 p.
  • Burnham K.P., Anderson D.R. & Huyvaert K.P. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons // Behavioral Ecology and Sociobiology. Vol.65. No.1. P.23–35.
  • Byers J.A. & Walker C. 1995. Refining the motor training hypothesis for the evolution of play // American Naturalist. Vol.146. No.1. P.25–40.
  • Caro T.M. 1981. Predatory behaviour and social play in kittens // Behaviour. Vol.76. No.1. P.1–24.
  • Caro T.M. 1995. Short-term costs and correlates of play in cheetahs // Animal Behaviour. Vol.49. No.2. P.333–345.
  • Cordoni G. 2009. Social play in captive wolves (Canis lupus): not only an immature affair // Behaviour. Vol.146. No.10. P.1363–1385.
  • Cordoni G., Norscia I., Bobbio M. & Palagi E. 2018. Differences in play can illuminate differences in affiliation: A comparative study on chimpanzees and gorillas // PLoS ONE. Vol.13. No.3. e0193096.
  • De Oliveira C.R., Ruiz-Miranda C.R., Kleiman D.G. & Beck B.B. 2003. Play behavior in juvenile golden lion tamarins (Callitrichidae: Primates): organization in relation to costs // Ethology. Vol.109. No.7. P.593–612.
  • Donaldson T.M., Newberry R.C., Špinka M. & Cloutier S. 2002. Effects of early play experience on play behaviour of piglets after weaning // Applied Animal Behaviour Science. Vol.79. No.3. P.221–231.
  • Drea C.M., Hawk J.E. & Glickman S.E. 1996. Aggression decreases as play emerges in infant spotted hyaenas: preparation for joining the clan // Animal Behaviour. Vol.51. No.6. P.1323–1336.
  • Driscoll C.A., Macdonald D.W. & O’Brien S.J. 2009. From wild animals to domestic pets, an evolutionary view of domestication // Proceedings of the National Academy of Sciences of the USA. Vol.106. Suppl.1. P.9971–9978.
  • Drummond H. 2006. Dominance in vertebrate broods and litters // Quarterly Review of Biology. Vol.81. No.1. P.3–32. Fagen R. 1981. Animal play behavior New York: Oxford University Press. 684 p.
  • Fagen R. & Fagen J. 2004. Juvenile survival and benefits of play behaviour in brown bears, Ursus arctos // Evolutionary Ecology Research. Vol.6. P.89–102.
  • Hager R., Cheverud J.M. & Wolf J.B. 2009. Change in maternal environment induced by cross-fostering alters genetic and epigenetic effects on complex traits in mice // Proceedings of the Royal Society, B: Biological Sciences. Vol.276. No.1669. P.2949–2954.
  • Held S.D.E. & Špinka M. 2011. Animal play and animal welfare // Animal Behaviour. Vol.81. No.5. P.891–899.
  • Heptner V.H. & Sludskii A.A. 1972. [Carnivores (Feloidea)]. Moscow: Vysshaya Shkola. 550 p. [In Russian].
  • Himmler B.T., Stryjek R., Modlinska K., Derksen S.M., Pisula & Pellis S.M. 2013. How domestication modulates play behavior: a comparative analysis between wild rats and a laboratory strain of Rattus norvegicus // Journal of Comparative Psychology. Vol.127. No.4. P.453–464.
  • Kitchener A.C., Breitenmoser-Würsten C., Eizirik E., Gentry A., Werdelin L., Wilting A., Yamaguchi N., Abramov A.V., Christiansen P., Driscoll C.A., Duckworth J.W., Johnson W.E., Luo S.J., Meijaard E., O’Donoghue P., Sanderson J., Seymour K., Bruford M.W., Groves C., Hoffmann M., Nowell K., Timmons Z. & Tobe S.S. 2017. A revised taxonomy of the Felidae. The final report of the Cat Classification Task Force of the IUCN/SSC Cat Specialist Group // CAT News. No.11. P.1-80.
  • Krachun C., Rushen J. & de Passillé A.M. 2010. Play behaviour in dairy calves is reduced by weaning and by a low energy intake // Applied Animal Behaviour Science. Vol.122. No.2–4. P.71–76.
  • Kuehl H.S., Elzner C., Moebius Y., Boesch C. & Walsh P.D. 2008. The price of play: self-organized infant mortality cycles in chimpanzees // PLoS ONE. Vol.3. No.6. e2440.
  • Lee P.C. & Moss C.J. 2014. African elephant play, competence and social complexity // Animal Behavior and Cognition. Vol.1. No.2. P.144–156.
  • Lenth R. 2016. Package ‘lsmeans’ http://cran.cnr.berkeley.edu/ web/packages/lsmeans/lsmeans.pdf
  • Leyhausen P.& Tonkin B.A. 1979. Cat behaviour. The predatory and social behaviour of domestic and wild cats. New York: Garland STPM Press. 340 p.
  • Llamazares-Martín C., Scopa C., Guillén-Salazar F. & Palagi E. 2017. Strong competition does not always predict play asymmetry: the case of South American sea lions (Otaria flavescens) // Ethology. Vol.123. No.4. P.270–282.
  • Luchetti A., Oddi D., Lampis V., Centofante E., Felsani A., Battaglia M. & D’Amato F.R. 2015. Early handling and repeated cross-fostering have opposite effect on mouse emotionality // Frontiers in behavioral neuroscience. Vol.9. P.93.
  • Martin P.& Bateson P. 1985. The influence of experimentally manipulating a component of weaning on the development of play in domestic cats // Animal Behaviour. Vol.33. No.2. P.511–518.
  • Martin P.& Bateson P. 1993. Measuring behaviour. An Introductory guide. Cambridge: Cambridge University Press. 222 p.
  • Matyushkin E.N. & Vaisfeld M.A. 2003. [The lynx. Regional features of ecology, use and protection]. Moscow: Nauka. 523 p. [In Russian].
  • McPhee M.E. & Carlstead K. 2010. The importance of maintaining natural behaviors in captive mammals // Kleiman D.G. et al. (eds.) Wild mammals in captivity: Principles and techniques for zoo management. Chicago: University of Chicago Press. P.303–313.
  • Meaney M.J., Stewart J. & Beatty W.W. 1985. Sex differences in social play: the socialization of sex roles // Advances in the Study of Behavior. Vol.15. P.1–58.
  • Mendl M. 1988. The effects of litter size variation on mother-offspring relationships and behavioural and physical development in several mammalian species (principally rodents) // Journal of Zoology. Vol.215. P.15–34.
  • Mendoza D.L. & Ramirez J.M. 1987. Play in kittens (Felis domesticus) and its association with cohesion and aggression // Bulletin of the Psychonomic Society. Vol.25. No.1. P.27–30.
  • Molinari P.& Molinari-Jobin A. 2001. Behavioural observations of interactions in a free-ranging lynx Lynx lynx family at kills // Acta Theriologica. Vol.46. No.4. P.441–445.
  • Naidenko S.V. 2001. Aggression in lynx adults-cubs relations: can it be a reason of litters dissolution? // Ethology Ecology & Evolution. Vol.13. No.3. P.283–295.
  • Naidenko S.V. 2005. [Features of reproduction and postnatal development of Eurasian lynx] Moscow: KMK Scientific Press. 112 p. [In Russian, with English summary].
  • Naidenko S.V. & Antonevich A.L. 2009. Sibling aggression in Eurasian lynx (Lynx lynx) // Vargas A. (ed.) Iberian Lynx Ex-situ Conservation: An Interdisciplinary Approach. Madrid, Spain: Fundación Biodiversidad. P.146–155.
  • Natoli E., Say L., Cafazzo S., Bonanni R., Schmid M. & Pontier 2005. Bold attitude makes male urban feral domestic cats more vulnerable to feline immunodeficiency virus // Neuroscience & Biobehavioral Reviews. Vol.29. No.1. P.151–157.
  • Norscia I. & Palagi E. 2011. When play is a family business: adult play, hierarchy, and possible stress reduction in common marmosets // Primates. Vol.52. No.2. P.101–104.
  • Nowell K. & Jackson P. 1996. Wild Cats. Status Survey and Conservation Action Plan. IUCN/SSC Cat Specialist Group. Gland: IUCN. 382 p.
  • Ottoni E.B. 2000. EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions // Behavior Research Methods, Instruments & Computers. Vol.32. No.3. P.446–449.
  • Palagi E., Burghardt G.M., Smuts B., Cordoni G., Dall’Olio S., Fouts H.N., Řeháková-Petrů M., Siviy S.M. & Pellis S.M. 2016a. Rough-and-tumble play as a window on animal communication // Biological Reviews. Vol.91. No.2. P.311–327.
  • Palagi E. & Cordoni G. 2012. The right time to happen: Play developmental divergence in the two Pan species // PLoS ONE. Vol.7. No.12. e52767.
  • Palagi E., Cordoni G., Demuru E. & Bekoff M. 2016b. Fair play and its connection with social tolerance, reciprocity and the ethology of peace // Behaviour. Vol.153. No.9–11. P.1195–1216.
  • Paquette D. 1994. Fighting and playfighting in captive adolescent chimpanzees // Aggressive Behavior. Vol.20. No.1. P.49–65.
  • Pellis S.M. & Iwaniuk A.N. 1999. The roles of phylogeny and sociality in the evolution of social play in muroid rodents // Animal Behaviour. Vol.58. No.2. P.361–373.
  • Poirier F.E. & Smith E.O. 1974. Socializing Functions of Primate Play // American Zoologist. Vol.14. No.1. P.275–287. Rutovskaya M.V. & Naidenko S.V. 2006. [Acoustic communication of lynx (Lynx lynx)] // Bulletin MOIP. Vol.111. No.1. P.3–9 [in Russian, with English summary].
  • Sharpe L.L. 2005. Play does not enhance social cohesion in a cooperative mammal // Animal Behaviour. Vol.70. No.3. P.551–558.
  • Sharpe L.L. & Cherry M.I. 2003. Social play does not reduce aggression in wild meerkats // Animal Behaviour. Vol.66. No.5. P.989–997.
  • Sidorovich V., Gouwy J. & Rotenko I. 2018. Unknown Eurasian lynx Lynx lynx: new findings on the species ecology and behaviour. Minsk: Minsk Chatyry Chverci. 276 p.
  • Sokolov V.E., Naidenko S.V. & Serbenyuk M.A. 1994. Specific fights of young lynxes (Felis lynx, Carnivora, Felidae) // Zoologicheskii Zhurnal. Vol.73. No.1. P.132–138 [in Russian with English summary].
  • Trut L.N., Plyusnina I.Z. & Oskina I.N. 2004. An experiment on fox domestication and debatable issues of evolution of the dog // Russian Journal of Genetics. Vol.40. No.6. P.644–655.
  • Turner D.C. 2000. The domestic cat: The biology of its behaviour. Cambridge: Cambridge University Press. 256 p.
  • Fagen R. 1981. Animal play behavior New York: Oxford University Press. 684 p.