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Use of social network models to understand play partner choice strategies in three primate species

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  • Social networks analysis in primates, a multilevel perspective
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Abstract

Although play is seen in many species, its evolutionary function is still largely unknown. Several relevant, proposed hypotheses (such as the training for the unexpected, self-assessment, social skills, and dominance hierarchy hypotheses) make predictions about how animals should optimally choose their play partners based on their familiarity or other demographic variables. We used a social network approach to analyze focal sample data on brown capuchins (Cebus apella), hamadryas baboons (Papio hamadryas), and diademed sifaka (Propithecus diadema) to understand how these species choose their play partners with respect to demographic variables. Using exponential random graph models (ERGMs), we found that sifaka and capuchins generally tended to play with animals who were similar to them. The baboons were only sensitive to age differences in the formation of strong play relationships. Our data most strongly support the training for the unexpected hypothesis, as according to predictions all species preferred to play with animals who were their close social partners, decreasing the possibility of cheating during play. Through the first application (to our knowledge) of ERGMs to primate behavior, we were able to compare the effects of many demographic variables on the complex, interdependent social structure of primates. Applying this tool to additional groups and species will provide further insight into evolutionary mechanisms of play behavior across taxa.

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References

  • Albers PCH, De Vries H (2001) Elo-rating as a tool in the sequential estimation of dominance strengths. Anim Behav 61:489–495

    Article  Google Scholar 

  • Amann AL, Pines M, Swedell L (2017) Contexts and consequences of takeovers in hamadryas baboons: female parity, reproductive state, and observational evidence of pregnancy loss. Am J Primatol 79(7):e22649. https://doi.org/10.1002/ajp.22649

  • Antonacci D, Norscia I, Palagi E (2010) Stranger to familiar: wild strepsirhines manage xenophobia by playing. PLoS One 5(10):e13218. https://doi.org/10.1371/journal.pone.0013218

  • Balasubramaniam KN, Beisner BA, Berman CM, De Marco A, Duboscq J, Koirala S, Majolo B, MacIntosh AJ, McFarland R, Molesti S, Ogawa H, Petit O, Schino G, Sosa S, Sueur C, Thierry B, de Waal FBM, McCowan B (2018) The influence of phylogeny, social study, and sociodemographic factors on macaque social network structure. Am J Primatol 80:e22727

    Article  Google Scholar 

  • Barber N (1991) Play and energy regulation in mammals. Q Rev Biol 66:129–147

    Article  CAS  PubMed  Google Scholar 

  • Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (2000) Female baboons give as good as they get, but do not raise the stakes. Anim Behav 59:763–770

    Article  CAS  PubMed  Google Scholar 

  • Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs, Canis familiaris. Anim Behav 73:489–499

    Article  Google Scholar 

  • Bekoff M (2001) Social play behaviour—cooperation, fairness, trust, and the evolution of morality. J Conscious Stud 8:81–90

    Google Scholar 

  • Bekoff M (2004) Wild justice and fair play: cooperation, forgiveness, and morality in animals. Biol Philos 19:489–520

    Article  Google Scholar 

  • Bekoff M, Beyers JA (1981) A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: an ethological hornet’s nest. In: Immelmann K, Barlow GW, Petrinovich L, Main M (eds) Behavioral development: the Bielefeld Interdisciplinary Project. Cambridge University Press, Cambridge, pp 296–337

  • Berger J (1980) The ecology, structure, and functions of social play in bighorn sheep (Ovis canadensis). J Zool 192:531–542

    Article  Google Scholar 

  • Blumstein DT, Chung LK, Smith JE (2013) Early play may predict later dominance relationships in yellow-bellied marmots (Marmota flaviventris). Proc R Soc Biol Sci. https://doi.org/10.1098/rspb.2013.0485

    Article  Google Scholar 

  • Brent LJN, MacLarnon A, Platt ML, Semple S (2013) Seasonal changes in the structure of rhesus macaque social networks. Behav Ecol Sociobiol 67:349–359

    Article  PubMed  Google Scholar 

  • Burghardt G (2005) The genesis of animal play: testing the limits. MIT Press, Cambridge

    Book  Google Scholar 

  • Butts C (2008) network: A package for managing relational data in R. J Stat Softw 24:1–36

    PubMed  PubMed Central  Google Scholar 

  • Butts C (2015) Network: classes for relational data. The Statnet project; R package version 1.13.0. http://statnet.org; http://CRAN.R-project.org/package=network. Accessed 15 Oct 2018

  • Butts C (2016) sna: Tools for social network analysis. R package version 2.4. http://CRAN.R-project.org/package=sna. Accessed 15 Oct 2018

  • Cafazzo S, Marshall-Pescini S, Essler JL, Virányi Z, Kotrschal K, Range F (2018) In wolves, play behaviour reflects the partners’ affiliative and dominance relationship. Anim Behav 141:137–150

    Article  PubMed  PubMed Central  Google Scholar 

  • Caro TM (1995) Short-term costs and correlates of play in cheetahs. Anim Behav 49:333–345

    Article  Google Scholar 

  • Cheney DL (1978) The play partners of immature baboons. Anim Behav 26:389–408

    Article  Google Scholar 

  • Ciani F, Dall’Olio S, Stanyon R, Palagi E (2012) Social tolerance and adult play in macaque societies: a comparison with different human cultures. Anim Behav 84:1313–1322

    Article  Google Scholar 

  • de Waal FBM (1991) Rank distance as a central feature of rhesus monkey social organization: a sociometric analysis. Anim Behav 41:383–395

    Article  Google Scholar 

  • Erhart EM, Overdorff DJ (2008) Rates of agonism by diurnal lemuroids: implications for female social relationships. Int J Primatol 29:1227–1247

    Article  Google Scholar 

  • Essler JL, Cafazzo S, Marshall-Pescini S, Viranyi Z, Kotrschal K, Range F (2016) Play behavior in wolves: using the ‘50:50’ rule to test for egalitarian play styles. PLoS One 11:e0154150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fady JC (1969) Social play: playmates chosen by young monkeys. Observations on Macaca irus. Folia Primatol 11:134–143

    Article  CAS  Google Scholar 

  • Fagen R (1981) Animal play behavior. Oxford University Press, Oxford

    Google Scholar 

  • Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol Evol 4:1187–1194

    Article  Google Scholar 

  • Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • Farine DR, Whitehead H (2015) Constructing, conducting, and interpreting animal social network analysis. J Anim Ecol 84:1144–1163

    Article  PubMed  PubMed Central  Google Scholar 

  • Fisher DN, Ilany A, Silk MJ, Tregenza T (2017) Analysing animal social network dynamics: the potential of stochastic actor-oriented models. J Anim Ecol 86:202–212

    Article  PubMed  PubMed Central  Google Scholar 

  • Flack JC, Jeannotte LA, de Waal FBM (2004) Play signaling and the perception of social rules by juvenile chimpanzees (Pan troglodytes). J Comp Psychol 118:149–159

    Article  PubMed  Google Scholar 

  • Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, Cambridge

    Google Scholar 

  • Goodreau SM, Kitts JA, Morris M (2009) Birds of a feather, or friend of a friend? Using exponential random graph models to investigate adolescent social networks. Demography 46:103–125

    Article  PubMed  PubMed Central  Google Scholar 

  • Govindarajulu P, Hunte W, Vermeer LA, Horrocks JA (1993) The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): the function of early play. Int J Primatol 14:701–719

    Article  Google Scholar 

  • Graham KL, Burghardt GM (2010) Current perspectives on the biological study of play: signs of progress. Q Rev Biol 85:393–418

    Article  PubMed  Google Scholar 

  • Handcock MS, Robins G, Snijders TAB, Moody J, Besag J (2003) Assessing degeneracy in statistical models of social networks. J Am Stat Assoc 76:33–50

    Google Scholar 

  • Handcock M, Hunter D, Butts C, Morris M (2008) statnet: Software tools for the representation, visualization, analysis and simulation of network data. J Stat Softw 24:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Handcock M, Hunter D, Butts C, Goodreau S, Krivitsky P, Bender-deMoll S, Morris M (2016) statnet: software tools for the statistical analysis of network data. The Statnet Project; R package version 2016.9. http://www.statnet.org; http://CRAN.R-project.org/package = statnet. Accessed 15 Oct 2018

  • Handcock M, Hunter D, Butts C, Goodreau S, Krivitsky P, Morris M (2018) ergm: Fit, simulate, and diagnose exponential-family models for networks. The Statnet Project; R package version 3.9.0-3896. http://www.statnet.org; https://CRAN.R-project.org/package=ergm. Accessed 15 Oct 2018

  • Hanneke S, Fu W, Xing EP (2010) Discrete temporal models of social networks. Electron J Stat 4:585–605

    Article  Google Scholar 

  • Hausfater G (1976) Predatory behavior of yellow baboons. Behaviour 56:44–68

    Article  Google Scholar 

  • Henkel S, Heistermann M, Fischer J (2010) Infants as costly social tools in male Barbary macaque networks. Anim Behav 79:1199–1204

    Article  Google Scholar 

  • Hunter D, Handock M, Butts C, Goodreau S, Morris M (2008) ergm: A package to fit, simulate and diagnose exponential-family models for networks. J Stat Softw 24:1–29

    Article  PubMed  PubMed Central  Google Scholar 

  • Imakawa S (1990) Playmate relationships of immature free-ranging Japanese monkeys at Katsuyama. Primates 31:509–521

    Article  Google Scholar 

  • Irwin M (2008) Feeding ecology of Propithecus diadema in forest fragements and continuous forest. Int J Primatol 29:95–115

    Article  Google Scholar 

  • Izawa K (1980) Social behavior of the wild black-capped capuchin (Cebus apella). Primates 21:443–467

    Article  Google Scholar 

  • Janson C, Baldovino MC, di Bitett M (2012) The group life cycle and demography of brown capuchin monkeys (Cebus [apella] nigritus) in Iguazu National Park, Argentina. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 185–212

  • Janus M (1989) Reciprocity in play, grooming, and proximity in sibling and nonsibling young rhesus monkeys. Int J Primatol 10:243–261

    Article  Google Scholar 

  • Judge PG, Mullen SH (2005) Quadriatic postconflict affiliation among bystanders in a hamadryas baboon group. Anim Behav 69:1345–1355

    Article  Google Scholar 

  • Kerridge FJ (2005) Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata). Am J Primatol 66:71–84

    Article  PubMed  Google Scholar 

  • Khan BN (2013) Impact of captivity on social behaviour of chimpanzee (Pan troglodytes). J Anim Plant Sci 23:779–785

    Google Scholar 

  • Krause J, James R, Franks DW, Croft DP (2014) Animal social networks. Oxford University Press, Oxford

    Book  Google Scholar 

  • Krivitsky PN (2012) Exponential-family random graph models for valued networks. Electron J Stat 6:1100–1128

    Article  PubMed  PubMed Central  Google Scholar 

  • Krivitsky P (2016) ergm.count: fit, simulate and diagnose exponential-family models for networks with count edges. The Statnet project; R package version 3.2.2. http://www.statnet.org; http://CRAN.R-project.org/package=ergm.count. Accessed 15 Oct 2018

  • Kummer H (1968) Social organization in hamadryas baboons: a field study. University of Chicago Press, Chicago

    Google Scholar 

  • Kummer H, Kurt F (1965) A comparison of social behavior in captive and wild hamadryas baboons. In: Vagtborg H (ed) The baboon in medical research. University of Texas Press, Austin, pp 65–80

    Google Scholar 

  • Leinfelder I, de Vries H, Deleu R, Nelissen M (2001) Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons. Am J Primatol 55:25–42

    Article  CAS  PubMed  Google Scholar 

  • LeResche LA (1976) Dyadic play in hamadryas baboons. Behaviour 57:190–205

    Article  Google Scholar 

  • Lusher D, Koskinen J, Robins G (eds) (2013) Exponential random graph models for social networks. Cambridge University Press, New York

  • Lutz MC, Judge PG (2017) Self-handicapping during play fighting in capuchin monkeys (Cebus apella). Behaviour 154:909–938

    Article  Google Scholar 

  • Martin P (1984) The time and energy costs of play-behavior in the cat. J Comparative Ethol 64:298–312

    Google Scholar 

  • Morris M, Handcock MS, Hunter DR (2008) Specification of exponential-family random graph models: terms and computational aspects. J Stat Softw 24:1548–7660

    Article  PubMed  PubMed Central  Google Scholar 

  • National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. National Academy Press, Washington, DC

  • Neumann C, Duboscq J, Dubuc C et al (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921

  • Noe R, Hammerstein P (1994) Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism, and mating. Behav Ecol Sociobiol 35:1–11

    Article  Google Scholar 

  • Palagi E, Paoli T, Tarli SB (2006) Short-term benefits of play behavior and conflict prevention in Pan paniscus. Int J Primatol 27:1257–1270

    Article  Google Scholar 

  • Paquette D (1994) Fighting and playfighting in captive adolescent chipmanzees. Aggress Behav 20:49–65

    Article  Google Scholar 

  • Paukner A, Suomi SJ (2008) Sex differences in play behavior in juvenile tufted capuchin monkeys (Cebus apella). Primates 49:288–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Paxton R, Basile BM, Adachi I, Suzuki WA, Wilson ME, Hampton HH (2010) Rhesus monkeys (Macaca mulatta) rapidly learn to select dominant individuals in videos of articial social interactions between unfamiliar conspecifics. J Comp Psychol 124:395–401

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 15 Oct 2018

  • Reed C, O’Brien TG, Kinnaird MF (1997) Male social behavior and dominance hierarchy in the Sulawesi crested black macaque (Macaca nigra). Int J Primatol 18:247–260

    Article  Google Scholar 

  • Robins G, Pattison P, Kalish Y, Lusher D (2007) An introduction to exponential random graph (p*) models for social networks. Soc Netw 29:173–191

    Article  Google Scholar 

  • Schaller GB (1972) The Serengeti lion. University of Chicago Press, Chicago

  • Seyfarth RM, Cheney DL (2003) The structure of social knowledge in monkeys. In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, pp 207–229

    Google Scholar 

  • Sharpe LL (2005) Play does not enhance social cohesion in a cooperative mammal. Anim Behav 70:551–558

    Article  Google Scholar 

  • Shimada M, Sueur C (2014) The importance of social play network for infant or juvenile wild chimpanzees at Mahale Mountains National Park, Tanzania. Am J Primatol 76:1025–1036

    Article  PubMed  Google Scholar 

  • Shimada M, Sueur C (2018) Social play among juvenile wild Japanese macaques (Macaca fuscata) strengthens their social bonds. Am J Primatol 80:e22728

    Article  Google Scholar 

  • Silk MJ, Fisher DN (2017) Understanding animal social structure: exponential random graph models in animal behaviour research. Anim Behav 132:137–146

    Article  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female bonds enhance infant survival. Science 302:1231–1234

    Article  CAS  PubMed  Google Scholar 

  • Smith EO (ed) (1978) Social play in primates. Academic, New York

  • Spinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168

    Article  CAS  PubMed  Google Scholar 

  • Stadele V, Pines M, Swedell L, Vigilant L (2016) The ties that bind: maternal kin bias in a multilevel primate society despite natal dispersal by both sexes. Am J Primatol 78:731–744

    Article  PubMed  Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Tecot SR, Gerber BD, King SJ, Verdolin JL, Wright PC (2013) Risky business: sex differences in mortality and dispersal in a polygynous, monomorphic lemur. Behav Ecol 24:987–996

    Article  Google Scholar 

  • Thompson KV (1996) Play-partner preferences and the function of social play in infant sable antelope, Hippotragus niger. Anim Behav 52:1143–1155

    Article  Google Scholar 

  • 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, pp 183–204

    Chapter  Google Scholar 

  • Visalberghi E, Guidi C (1998) Play behaviour in young tufted capuchin monkeys. Folia Primatol 69:419–422

    Article  CAS  Google Scholar 

  • Watson DM, Croft DB (1996) Age-related differences in playfighting strategies of captive male red-necked wallabies (Macropus rufogriseus banksianus). Ethology 102:336–346

    Article  Google Scholar 

  • Weir JS (2014) Infant development and maternal strategies in the two largest lemurs: the diademed sifaka (Propithecus diadema) and the indri (Indri indri). Dissertation. University of Victoria, Victoria

  • Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) GLM and GAM for count data. In: Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (eds) Mixed effect models and extensions in ecology with R. Springer, New York, pp 209–243

    Chapter  Google Scholar 

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Acknowledgements

We would like to thank Mary Gavitt, Gretchen Long, Amber Hackenberg, and the rest of Bucknell’s animal caretakers for their excellent care of all the monkeys at the Bucknell Animal Behavior Laboratory. We would also like to thank Ravi Goyal, Mathematica, for his advice on the analysis. We would like to thank the entire GERP team in Antananarivo, Madagascar for their help in organizing research permits, and the Maromizaha team in Anevoka for arranging logistics while on site. Data collection in the field was supported by MAMINIRIMA Herinjetovo and RANDIANATOANDRO Heritiana. Additional dominance data was collected by Corinne Leard, Allie Schrock, Melissa Painter, Danielle Antonellis, and Amelia Lautenberg. We also thank Dr. Matthew Silk and two anonymous reviewers for their helpful comments on earlier drafts of the manuscript. Thanks also to Mark Grote for helpful guidance on aspects of the analysis during the review process and to Damien Caillaud, Alexandra McInturf, and Neetha Iyer for helpful discussions on the manuscript revisions. MCL was supported by a Bucknell Program for Undergraduate Research Grant, two Bucknell University Animal Behavior summer research grants, a Bucknell University Statistics summer research grant, and a Bucknell University Presidential Fellowship. The primate facility was supported by Bucknell University.

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Authors and Affiliations

  1. Animal Behavior Program, Bucknell University, Lewisburg, USA

    Meredith C. Lutz & Peter G. Judge

  2. Department of Mathematics, Bucknell University, Lewisburg, USA

    Meredith C. Lutz

  3. Animal Behavior Graduate Group, University of California, Davis, c/o Young Hall Room 330, 1 Shields Avenue, Davis, CA, 95616, USA

    Meredith C. Lutz

  4. Le Groupe d’Étude et de Recherche sur les Primates de Madagascar (GERP), 34 Cité des Professeurs, Fort Duchesne, 101, Antananarivo, Madagascar

    Meredith C. Lutz & Jonah Ratsimbazafy

  5. Department of Paleontology and Anthropology, University of Antananarivo, 101, Antananarivo, Madagascar

    Jonah Ratsimbazafy

  6. Department of Psychology, Bucknell University, 1 Dent Drive, Lewisburg, PA, 17837, USA

    Peter G. Judge

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  1. Meredith C. Lutz
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Correspondence to Meredith C. Lutz.

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Lutz, M.C., Ratsimbazafy, J. & Judge, P.G. Use of social network models to understand play partner choice strategies in three primate species. Primates 60, 247–260 (2019). https://doi.org/10.1007/s10329-018-00708-7

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