Playing it cool: Characterizing social play, bout termination, and candidate play signals of juvenile and infant Tibetan macaques (Macaca thibetana)

2018·0.42 MB·

by  Wright, Kaitlin R

ZOOLOGICAL RESEARCH
Playing it cool: Characterizing social play, bout
termination, and candidate play signals of juvenile and
infant Tibetan macaques (Macaca thibetana)
KaitlinR.Wright1,JessicaA.Mayhew1,2,LoriK.Sheeran1,2,JakeA.Funkhouser1,Ronald. S.Wagner1,3,Li-XingSun1,3,
Jin-HuaLi4,*
1PrimateBehaviorandEcologyProgram,CentralWashingtonUniversity,EllensburgWashington98926,USA
2DepartmentofAnthropology,CentralWashingtonUniversity,EllensburgWashington98926,USA
3DepartmentofBiologicalSciences,CentralWashingtonUniversity,EllensburgWashington98926,USA
4SchoolofResourceandEnvironmentalEngineering,AnhuiUniversity,HefeiAnhui230601,China
ABSTRACT juvenileandinfantmacaquesusedmultiplebodyand
facial candidate play signals. Our data showed that
Playbehaviorsandsignalsduringplayfulinteractions juvenileandinfantTibetanmacaquesuseaversatile
with juvenile conspecifics are important for both the repertoireofplaybehaviorsandsignalstosustainplay.
social and cognitive development of young animals.
Keywords: Social play; Play signaling; Play face;
Thesocialorganizationofaspeciescanalsoinfluence
Macacathibetana
juvenile social play. We examined the relationships
INTRODUCTION
among play behaviors, candidate play signals, and
playboutterminationinTibetanmacaques(Macaca Playisoneofthemostconspicuousbehaviorsinwhichanimals
thibetana) during juvenile and infant social play to engage. Social play combines elements of cooperation,
communication, and reciprocity in participant actions. Play
characterize the species play style. As Tibetan
also incorporates behavioral modifications from other social
macaques are despotic and live in groups with
contexts, such as agonism, mating, and predation, and
strict linear dominance hierarchies and infrequent
thus the division between play and non-play is not always
reconciliation,wepredictedthatplaywouldbeatrisk obvious (Burghardt, 2005). Although play behavior has been
of misinterpretation by both the individuals engaged researchedformanydecades,itisvariouslydefineddepending
in the play bout and by those watching, possibly on the field of study from which it is viewed. For example,
Fagen (1981) defined play as behavior that “functions to
leading to injury of the players. Animals living in
develop,practice,ormaintainphysicalorcognitiveabilitiesand
such societies might need to frequently and clearly
social relationships,includingbothtactics and strategies, by
signalplayfulintenttoplaypartnersandothergroup
memberstoavoidaggressiveoutcomes. Wegathered
video data on 21 individually-identified juvenile and
Received: 31October2017;Accepted: 12April2018;Online: 04May
infant macaques (one month to five years of age) 2018
fromtheValleyoftheWildMonkeys,Mt. Huangshan, Foundation items: This project was supported by grants from
China. We used all-occurrence sampling to record Debra and Arlen Prentice, Central Washington University School
play behaviors and candidate play signals based of Graduate Studies and Research, National Science Foundation
on an ethogram. We predicted that play groups (NSF)InternationalResearchExperiencesforStudents(IRES)(OISE
wouldusemultiplecandidateplaysignalsinavariety 1065589), and National Science Foundation of China (31372215,
of contexts and in association with the number of 31672307)
audiencemembersinproximitytotheplayersandplay *Correspondingauthor,E-mail:[email protected]
boutlength. Inthe283playfulinteractionswescored, DOI:10.24272/j.issn.2095-8137.2018.048
272 SciencePress ZoologicalResearch39(4):272–283,2018
varying, repeating, and/or recombining already functional behaviorsandisincompleteorexaggerated; (4)isperformed
subsequences of behavior outside their primary context” (p. repeatedly but not stereotypically; and (5) occurs when the
65).Fagen’sdefinitionfocusesonplayfunction;however,even organism is free of stress or social/physical pressures (i.e.,
todaytheultimatebenefitsofplayremaincontroversial. From the player is in a “relaxed field”). Burghardt (2005) further
astructuralperspective,Burghardt(2005)proposedaworking posited that these criteria must be met to label a behavior as
definition for identifying play behaviors using five key criteria: playfulinsolitaryorsocialcontexts. Fagen’sdefinitionofplay
that is, play behavior (1) has limited immediate function; (2) behavior,coupledwithBurghardt’scriteriaforidentifyingthese
hasanendogenouscomponentthatisvoluntary,rewarding,or behaviors, offer a method to recognize and characterize play
autotelic;(3)isstructurallyortemporallydifferentfrom“serious” versusnon-playbehaviorinanimalsofallages(Table1).
Table1Operationaldefinitions
Term Definition
Functionstodevelop,practice,ormaintainphysicalorcognitiveabilitiesandsocialrelationships,
Playbehavior includingbothtacticsandstrategies,byvarying,repeating,and/orrecombiningalreadyfunctional
sub-sequencesofbehavioroutsidetheirprimarycontext(Fagen,1981,p65).
Communicatorybehaviorsthatfunctiontopromote,cultivate,andmanagesocialplayand
Playsignal
demonstrateplayfulintentions(Bekoff,1974;Fagen,1981;Yanagi&Berman,2014a,2014b).
Successfulbout Startoftheboutmarkedbyexchangeofphysicalcontact,chasing,orotherplaytypeorplaysignal.
Various solitary and social play behaviors are observed Thierry,2007).Despoticspecies,suchasJapanesemacaques
across animal species (e.g., turtles, Trionyx triunguis: (Macaca fuscata), with high rates of aggression, low rates of
Burghardt et al., 1996; elephants, Loxodonta Africana: Lee reconciliation, and high levels of nepotism are characterized
& Moss, 2014; domestic dogs, Canis familiaris: Horowitz, by a competitive, defensive, and low-risk play style (Petit et
2009);however,playisparticularlyimportanttoprimates,with al., 2008; Reinhart et al., 2010). Additionally, mothers in
relevancetosocialandcognitivedevelopment(Martin&Caro, despotic species may adopt a more restrictive rearing style,
1985; Palagi et al., 2007). Therefore, studying play can and mothers of low-ranking individuals may intervene when
provide important insight on a species’ social relationships, theiroffspringattempttoplaywiththeoffspringofhigh-ranking
how a species develops, and how they relate to cognitive females(Maestripieri,2004).Incontrast,speciesthataremore
abilities. Playing with juvenile and infant (hereafter: juvenile) egalitarian and characterized by low rates of aggression and
conspecifics is typically the first non-mother activity to occur high rates of affiliation and reconciliation, such as Tonkean
in young animals (Bekoff, 1972; Poirier, 1970). Playing macaques(Macacatonkeana),haveamorecooperative,close
with peers gradually increases in frequency, complexity, and contact play style and less restrictive mothers (Maestripieri,
intensity as juveniles age and their social networks expand. 2004; Petit et al., 2008; Reinhart et al., 2010). These play
The repetitive modification and practice of behaviors (e.g., patterndifferencesappeartovarywithsocialorganizationand
mounting and biting) within the play context may yield both exist due to the potential devolvement of play from a friendly
short- and long-term benefits in future hunting, mating, or interaction into an aggressive one that has likely negative
social interactions (Bekoff & Allen, 1997). The frequency of repercussions for the players. Variability in play frequency
playful behavior typically declines as juveniles transition into and form also extends to the individual level, in which an
adulthood, although adults may maintain playful relationships individual’s“playfulness”islikelyinfluencedbymultiplefactors,
with juveniles (e.g., geladas, Theropithecus gelada: Mancini including personality (Lampe et al., 2017; Pellis & McKenna,
& Palagi, 2009; chimpanzees, Pan troglodytes: Palagi et al., 1992), prior experience (Cloutier et al., 2013), opportunity to
2004; Shimada & Sueur, 2014). Less frequently, adult-adult play(Panksepp&Beatty,1980),andneurochemistry(Siviyet
play can occur in some primate species in both sexual and al.,2011). However,muchofthisresearchislimitedtohuman
non-sexualcontexts(Pellis&Iwaniuk,1999;T.gelada:Mancini children and laboratory rats; therefore, examining individual
&Palagi,2009;bonobos,P.paniscus: Palagi,2006;ring-tailed differences in playfulness across multiple species, including
lemurs, Lemur catta: Palagi, 2009; Pellis & Iwaniuk, 2000; P. primates,isnecessary.
troglodytes: Yamanashi et al., 2018) but may exhibit variable Social play fighting in juvenile animals may influence the
formsandfunctionsinspecieswithdifferentsocialorganization. development of dominance relationships later in life (Pellis
In primates, e.g., Macaca spp., social organization exerts & Pellis, 1996), and the style of play fighting may also be
a pervasive influence on a variety of behaviors, including related to a species’ social structure and dominance style
play (Ciani et al., 2012; Fagen, 1981; Maestripieri, 2004; (Fagen,1981;Palagi,2006;Petitetal.,2008).Althoughgentle
ZoologicalResearch39(4):272–283,2018 273
playfightingmaybeusedtomaintainaffiliation, moreintense multifunctionalandmayalsoworktomodulatemood(Pelliset
rough-and-tumble play may establish a dominance hierarchy al.,2011),inviteathirdpartyintotheplaybout,expressplayful
inpost-pubertaljuveniles(especiallyinmale-maleplaybouts) intenttoathirdparty, oractasarewardforbothpartnersfor
bytestingthestrengthofplayparticipants(Palagietal.,2007; playful engagement (Spijkerman et al., 1996). Play signals
Pellis & Pellis, 1996). Thus, play style may be predictive of likely perform a critical role in prolonging play duration and
socialdominancestyle,andthebalancebetweencooperation maintainingmultipleplayersinabout(polyadicplay).However,
andcompetitionwithinaplayboutmaybedifferentdepending it is possible that certain factors also decrease a signal’s
on the nature of a species’ social system (Palagi, 2006; Petit salience, including increase in bout length, bout intensity,
et al., 2008; Reinhart et al., 2010). An individual may use misdirectionorimpairmentofthesignal,changesinaudience
certain behaviors, such as slap or chase, to test, cultivate, or members, or the addition of more players (Bekoff, 1972).
stabilize a competitive edge in a play bout (van Leeuwen et Short play bouts may be influenced by the misinterpretation
al., 2011). By testing one’s competitive advantage against a of play signals and, similarly, long play bouts with aggressive
peerduringplay,partnerscanpracticeaggressiveinteractions behaviors, such as wrestling, may need to include a higher
thatmaybenecessarylaterinlifetodefend,maintain,orgain frequency of intention reinforcing play signals (Spijkerman et
accesstoresources. Moreover, thefrequencyofplayfighting al., 1996). Research reflects the variation and degree of
and use of play signals in certain social systems, such as frequency, flexibility, and functionality of play signals, which
the egalitarian social structure characteristic of adult female also appear to be influenced by species social organization.
bonobos(P.paniscus),mayindicatethenecessityofaflexible Therefore,possessingadiverserepertoireofsignals(suchas
playstyletoassessandstrengthensocialrelationships(Palagi, vocalizationsandheadandbodymovements),inadditiontothe
2006). iconicplayfaceorplaybow,maybeadvantageousforjuveniles
For many primates, social play is frequently coupled with tolearnandpractice;onemightexpectmultipleplaysignalsto
playfulsignalsobservedthroughoutaplaybout(Fagen,1981; haveevolvedinanygiventaxon.
Yanagi & Berman, 2014a). During play, partners transmit For the genus Macaca (23 species), visual signals during
and receive signals, which include vocalizations (Biben & play, such as bared teeth or play face, are used differently
Symmes, 1986; Kipper & Todt, 2002, Vettin & Todt, 2005), depending on the social organizational grade of the species
body movements, gestures, and/or facial expressions (e.g., (Scopa & Palagi, 2016; Thierry et al., 2000). For example,
relaxedopenmouthorplayface;Bekoff&Allen,1997;Pellis& bared teeth as a play signal might be held longer or
Pellis,1996).Thesesignalsmayfunctiontoqualifysubsequent performedmorefrequentlyinonespeciescomparedtoanother.
behaviors as playful, maintain a playful context, and/or help Macacaspeciessharesimilaritiesinsocialstructure,including
to avoid an escalation to aggression, especially when the multi-maleandmulti-femalegroups,overlappinghomeranges,
behaviors performed are risky or ambiguous (e.g., play bite, and female philopatry; however, interspecific variation can
play slap, or play fight; Bekoff & Allen, 1997; Burghardt, be found in patterns of affiliation, reconciliation, dominance,
2005; Pellis & Pellis, 1996). Play signals can therefore be aggression,nepotism,andtemperament(Thierry,1985,1990;
definedascommunicatorybehaviorsthatfunctiontopromote, Thierry et al., 2000). Macaques are categorized on a
cultivate, and manage social play and demonstrate playful 4-gradetolerancescale,withGrade1beinghighlyhierarchical,
intent (Bekoff, 1974; Fagen, 1981; Waller & Cherry, 2012; nepotistic, and despotic (e.g., M. mulatta or M. fuscata) and
Yanagi&Berman,2014a;Table1). Thereisdebatethatsuch Grade 4 being more tolerant or egalitarian (e.g., M. tonkeana
signals are only observed during the context of play and are or M. nigra) (Thierry et al., 2000). Tolerant macaque species
distinct from the behaviors used within a play bout, and also use play signals interchangeably and redundantly to initiate
predict the occurrence of play (Bekoff, 1974; Fagen, 1981; and/or terminate play and self-regulate mood (Pellis et al.,
Yanagi & Berman, 2014a). However, many potential signals 2011; Scopa & Palagi, 2016). They also engage in rapid
discussed in the literature (e.g., play bow in canids or play facial mimicry with their play partner, where one partner
face in primates) are unclear as indicators of the beginning mimics the facial expression of the other (Scopa & Palagi,
of a play bout; instead, these signals often punctuate the 2016). Suchmimicryisanunconsciousmotormirrorresponse
boutatdifferentpointsandarevariableintheirduration,form, and appears to contribute to increased play duration in more
and intensity. For example, the play face, also known as the tolerant species (Mancini et al., 2013; Scopa & Palagi, 2016;
relaxedopenmouthface,isafrequently-observedplaysignal see Palagi & Scopa, 2017 for discussion). This flexibility in
in primates and is commonly associated with close-quarter signaling may be related to an unpredictable but cooperative
contact, which occurs during play fights (Palagi et al., 2014; and less risky play style. Conversely, in despotic macaque
Pellis & Pellis, 1996; van Hooff, 1967). The intensity, rate, species, ambiguous play behaviors and miscommunication
and timing of the play face can change with the intensity or likely generate increased social repercussions and physical
behavioral content of the play interaction, thus acting as a risks; therefore, play signals may be particularly inflexible,
flexible message to indicate playful intent while the dynamics specific,andlessinterchangeableinsuchspeciesthatexhibit
of a bout quickly change (Pellis & Pellis, 1996; Špinka et al., highlevelsofaggressionandcompetitiveplaystyle(Scopa&
2016;Symons,1978;Waller&Cherry,2012;Waller&Dunbar, Palagi, 2016; Thierry et al., 2000; Yanagi & Berman, 2014b).
2005). Thisflexibilitysuggeststhattheplayfaceismostlikely In such cases, play signals may alert both participants and
274 www.zoores.ac.cn
third parties that the players are “only playing,” and may be as there are currently no published studies characterizing
performed more often when a third party, such as a related the specific play behaviors and signals observed during their
adult or juvenile conspecific, is present and participation or playful interactions. Insight on Tibetan macaque juvenile play
interferenceislikely(Pellisetal.,2011). will provide an important foundation to examine their social
In free-ranging despotic juvenile rhesus macaques (M. and cognitive development in relation to social structure and
mulatta), play signals predict the imminent occurrence of organization.
dyadic play (Yanagi & Berman, 2014a). Furthermore, most We characterized play behaviors and identified candidate
signals are non-randomly associated with various initiations play signals in juvenile Tibetan macaques. Tibetan
of play, indicating that signals are used selectively by the macaques show evidence of despotism, with a Grade 2
players depending upon the play content (Yanagi & Berman, social organization, linear dominance hierarchies, and low
2014b). For instance, chase play is often associated with conciliatory tendencies (Berman et al., 2004). It is expected
a crouch-and-stare signal, and leg-peeks are typically used that this despotic social structure will impact juvenile play
by the play recipient, not the initiator (Yanagi & Berman, behavior,playboutproximitytoadults(i.e.,potentialthird-party
2014b). For Grade 1 despotic macaques, the specific adult interference), frequency and distribution of play signals
use of signaling might decrease miscommunication and help performed by juveniles, and composition of players within the
reinforce,clarify,oremphasizetheplayfulintentofthesender, bout (i.e., audience members). Specifically, do juveniles use
wherebyindicatingthatparticipantsare“onlyplaying”alleviates specificcandidateplaysignalsinvariousplaycontextsbased
potentialrisingtensionwithinthegroup. Therefore,onemight on the length of the bout and number of audience members
hypothesize that multiple play signals may be used in other in proximity? We therefore tested the following predictions:
despoticmacaquespeciestoclarifysocialplaywhilemitigating 1) due to the despotic dominance style, third-party adult
potential associated aggression (Yanagi & Berman, 2014b). interference will end play more often than other forms of play
However,theextenttowhichthesesignalsarespecies-specific bouttermination(e.g., withdrawal)(Pellisetal.,2011; Thierry,
isunknown. 2011; Yanagi & Berman, 2014b); 2) play behaviors and play
Tibetan macaques (M. thibetana) are the largest macaque signals will show unequal distribution at the beginning of a
species and the most derived of their particular lineage bout, with play signals occurring more frequently to indicate
(Fooden, 1983; Thierry, 2011). Female macaques reach that the subsequent behaviors are playful (Yanagi & Berman,
adulthoodatapproximatelyfourorfiveyearsofage,generally 2014a); 3) the number of play bout audience members will
birththeirfirstoffspringbetweenfourandsixyearsofage,and be positively correlated with the number of observed play
nurse infants for six to twelve months (Zhao & Deng, 1988). signalsduetoanincreasednecessitytoconveyplayfulintent
In males, adulthood begins at approximately seven years of to more individuals (Bekoff, 1972; Spijkerman et al., 1996;
age (Zhao & Deng, 1988). Tibetan macaques reproduce Palagi,2006);and4)playdurationwillbepositivelycorrelated
seasonally, and the number of offspring sired by a male is with the number of observed play signals to reinforce, clarify,
correlated with his dominance rank (Thierry, 2011; Xia et andemphasizeplayfulintent(Pellis&Pellis,1996;Spijkerman
al., 2012). Tibetan macaque social organization consists of et al., 1996; Yanagi & Berman, 2014b). We also analyzed
multi-male, multi-female groups of 15–50 individuals, with a the distribution of playful behaviors and signals across all
female-skewed sex ratio (Berman et al., 2004; Li et al., 2007; individualsandinvestigatedthepossibleeffectsofsexandage
Thierry et al., 2000; Thierry, 2011). This organization is on the frequency of dyadic engagement in playful behaviors
centeredondominancehierarchiesandkin-bondedcoalitions andplaysignaling.
(Thierry, 2011). The dominance rank of females is based on
MATERIALSANDMETHODS
matrilines, with a daughter generally attaining the dominance
rankimmediatelybelowhermotherbutaboveheroldersiblings
Subjectsandstudysite
(Berman et al., 2004; Thierry, 2011; Zhao, 1997). This
Video data were collected on 21 individually-recognized,
hierarchy influences intergroup competition among females
free-ranging infant and juvenile Tibetan macaques of the
and preferential bonds between kin (Thierry, 2011). Most
Yulingkeng A1 (YA1) group located at the Valley of the Wild
males disperse at adulthood and transfer between groups
Monkeys in the Huangshan Scenic District, Anhui Province,
during their lifespan, regardless of dominance rank (Thierry,
China(seeBerman&Li,2002formoreinformationaboutthe
2011; Zhao, 1997). Although group males occupy the top
site). These individuals were between one month and five
ranks,femalescanoccasionallyoutrankmales(Bermanetal.,
yearsoldbasedonMacacaagecategorization(Thierry,2011)
2004). Adult social relationships influence the socialization
and current group structure maintained by the researchers of
of immature individuals (Thierry, 2011), with the population
Anhui University. At the time of the study (summer 2015),
generally showing a kin bias and linear hierarchies (Berman
10 juvenile males were present, including (4) five year olds,
et al., 2004). As such, it is expected that the Grade 2 social
(3) three year olds, (1) two year old, and (2) individuals less
organization of Tibetan macaques will affect juvenile play via
than 12 months old; and 11 juvenile females were present,
third-partyadultinterference, wherebyaggressiveoraffiliative
including:(1)fiveyearold;(3)threeyearolds;(4)twoyearolds,
behaviors are used to disrupt and terminate play. However,
and (3) individuals less than 12 months old. Data collection
little is known about the play style of Tibetan macaques,
focusedonjuvenilesasadult-adultplayisrareandmaydisplay
ZoologicalResearch39(4):272–283,2018 275
different frequencies of play signals than that which occurs video data. During preliminary data collection, inter-observer
during immature play (Mancini & Palagi, 2009; Palagi et al., reliabilityinindividualidentification(κ=0.86)andintra-observer
2004; Shimada & Sueur, 2014). The members of YA1 have reliability using play behavior and signal ethograms were
been habituated to human presence since 1986 for scientific established (play behavior: κ=0.93, play signals: κ=0.88,
researchandsince1992fortourism(seeBermanetal.,2004). bout termination: κ=1.00, actor identification: κ=0.87, and
The macaques at this site are provisioned with corn three to audience member identification: κ=0.86). All-occurrence
fourtimesdailybytheparkstaff,andthefeedingsarevisibleto sampling was used to efficiently record high quantity playful
tourists (see Berman & Li, 2002). The monkeys occasionally interactions(Altmann,1974).Allplayfulinteractionsdefinedby
interact with people (McCarthy et al., 2009). We obtained Fagen(1981)andoutlinedbyBurghardt(2005)wererecorded,
research approval from the Central Washington University including play behaviors (see Tables 1 and 2) and candidate
Institutional Animal Care and Use Committee (#A021507), play signals (see Tables 1 and 3), using a Canon HD Vixia
andourresearchprotocolsfollowedthelegalrequirementsof camcorder.Observationswereundertakenfromtourist-viewing
the People’s Republic of China and the American Society of platforms and near feeding sites and other locations where
Primatologists’PrinciplesfortheEthicalTreatmentofPrimates. juvenileandadultmacaqueswerevisible.Ifasecondplaybout
occurredsimultaneouslywhileobservingaprecedingplaybout,
Videodatacollection
onlyplaybehaviorsandsignalsintheinitialboutwererecorded.
Video data were collected at the study site from 3 August to
After the players disengaged from the play bout, recording
19September2015fromapproximately0800hto1800heach
continueduntil10shadelapsedwithoutboutre-initiation.
day, resulting in 48 d in the field and approximately 400 h of
Table2Definitionsandcomponentsofplaybehaviors
Typeofplay Behaviorcomponent Definition
Locomotiveactions,suchasrunning,climbing,and
leapingtowardsorawayfromanotherindividual,in
Chasing Leaping,running,walking
whichanimalsalternaterolesofchaserandchasee,
withouthavingbodycontactwitheachother.
Slightlyresembleswrestling,butinanextremely
Embracing,holding,hugging, mildform,i.e.,holdingeachotherwithveryslight
Cuddling
touching pushingofbody,butwithoutanybodydisplacement.
Oftenresemblesembracing.
Playinwhichanimalsgrappleandplacetheir
Biting,dragging,embracing,
mouthsoneachother’sbody.Typicallyinvolves
grabbing,hitting,leaping,lying,
Playbiting similarbehaviorpatternstowrestlingbutoccurswith
pinning,pulling,pushing,rolling,
biting.Bitingandavoidingbeingbittenwithbody
running,tackling,touching,walking
displacementarecentralactivities.
Twoanimalshiteachotherwiththeirhandsfora
Hittingwithhands,touching,
Slapping periodwithoutproceedingtoaclearerformofplay,
visualfixation
norterminatingtheplayencounter.
Dragging,embracing,grabbing, Alsoknownasrough-and-tumbleplay.Includes
hitting,leaping,lying,pinning, playbehaviorpatternsinwhichtwomonkeys
Wrestling
pulling,pushing,rolling,running, engageinmutualgrasping,pushing,pulling,
tackling,touching,walking androlling,withoutattemptstobiteeachother.
Ethogramforrhesusmacaque(Macacamulatta)play:Yanagi&Berman(2014a;2014b).
Videodataanalysis used to analyze the play bout video data, recording all play
Fromthevideofootage,thetimestamp,actoridentity,audience behavior and candidate play signals observed throughout all
member identity, and play signals and behaviors of the dyadicandpolyadicplaybouts. Behaviorspreviouslyunlisted
participants were coded (QuickTime Player for Mac). A by Yanagi & Berman (2014b) were added to the play signal
modified macaque ethogram (Yanagi & Berman, 2014b) was ethogram and included play threat and slap-and-play face
276 www.zoores.ac.cn
(Table 3). We estimated each player’s proximity to group the audience member tally was categorized as zero. In this
members as within arm’s reach (<50 cm) or beyond arm’s study,weconsideredplaybouts“successful”whenthestartof
reach (>50 cm). If a group member (adult or juvenile) was theboutwasmarkedbytheexchangeofcontact, chasing, or
in proximity to the play bout then he or she was considered otherplaybehaviors/signals(recordedas“startofplay”)(Table
partoftheplaybout’saudience,regardlessoftheirorientation 1). Asuccessfulplayboutwasconsidered“terminated”when
or activity. Each member of the play bout was counted to a player engaged in 1) non-play activities, e.g., grooming; 2)
generateanaudiencemembertally. Ifanindividualperformed withdrewfromthebout;or3)adultinterferenceoccurred(Table
aplaysignalorbehaviorwithoutagroupmemberinproximity, 4;recordedas“endofplay”).
Table3Definitionsofplaysignals
Playsignal Definition
Animal’sventralsurfaceison/neargroundanditslimbsarefixed,
Crouch-and-stare
whilemaintainingvisualfixationonpartner(Symons,1978).
Dangle-and-stare Animalstaresatpartnerwhilehangingfromanobjectbyhindlimbs(Levy,1979).
Bobbing,highsteppinggaitinwhichforequartersandhindquartersarealternately
Gamboling
raised(Symons,1978).Oftenaccompaniedbyrotationofthehead(Sade,1973).
Animalhidesbehindanobjectandthenpeeksatpartner,
Hide-and-peek
alternatingthetwobehaviorpatterns.
Animalstaresatpartnerthroughitslegswiththetopofitsheadagainsttheground
Leg-peek
(Symons,1978).Animalmayholditsanklesorplaceforearmsonground.
Animal’sbodyisorientedawayfrompartnerinafixedpositiononallfours,whilethe
Look-back
headisturnedtowardthepartnerovertheshoulder(Levy,1979;Symons,1978).
Playface Relaxed,openmouthface,typicallyobservedduringplaybouts(Levy,1979).
Roll-onto-back
Animalrollsandliesonitsbackandstaresatpartner(Levy,1979).
-and-stare
Playthreat Animaldirectsalunge<2bodylengthstowardsanotherindividual,
(candidatesignal) endingthemovementbyhittingtheground,withoutfacialexpression.
Slap-and-playface Animalhitsanotherindividual’sbodywhilesimultaneously
(candidatesignal) directinganopenmouthfacetowardstheindividual.
AdaptedfromYanagi&Berman(2014b).
Table4Definitionsofplaybouttermination
Modeoftermination Definition
Playersbegintoengageinanybehavior/
Non-playactivities activitynotconsideredunderthecategory
orcriteriaofplay(Bermanetal.,2004).
Playersmoveoutofproximityfromeach
Withdraw other(outofarmsreach),andnosubsequent
playbehaviorsorsignalsareobserved.
Playboutisinterruptedbyanadultgroupmember
Adultinterference performingaggressiveornon-aggressivebehaviors
towardsanyplayer(Bermanetal.,2004).
AdaptedfromBermanetal.(2004).
ZoologicalResearch39(4):272–283,2018 277
Statisticalanalysis acrossindividuals.
UsingIBMSPSSStatistics(Version23),VassarStatsWebsite
Distributionofplayacrossageandsexclasses
forStatisticalComputations(©RichardLowry,1998–2013),and
We used MR-QAP regression analyses in UCINET to
UCINET (Borgatti et al., 2002), we tested each prediction
investigate possible correlations between the dyadic
with α=0.05. We only analyzed successful bouts and the
frequencies of play behaviors, play signals, age, and sex.
signals that were displayed during such bouts. We used
Being of the same age class had no effect on either the
chi-squaregoodnessoffitteststoassesspredictions1,2,and
dyadic frequency of playful behaviors (Y=–0.007X+0.86,
3. Spearman’s rank correlation tests were used to analyze
P=0.41,r2=0.00)orplaysignaling(Y=–0.008X+4.53,P=0.43,
the average number and rate (average number/min) of play
r2<0.001). However, being of the same sex was significantly
signalsacrossboutlength(prediction4).Additionally,weused
related to both the dyadic frequencies of playful behavior
chi-square goodness of fit tests to examine the distribution of
(Y=1.22X+0.54, P=0.025, r2=0.023) and play signaling
the total frequency of play signals across varying audience
(Y=16.91X+2.73,P=0.031,r2=0.017). Althoughtheseresults
numbers. We also used chi-squared goodness of fit tests to
showedthatsexhadasignificanteffectonplaybehaviorand
analyzethedistributionofplaybehaviorsandsignalsforeach
signaling, the sizes of these effects were small (r2<0.023).
individual. Spearman’scorrelationcoefficientwasusedtotest
Giventheseresults,wedidnotdividethesubsequentanalyses
the correlation between the number of observed play signals
intodifferentdyad-specificsexorageclasses.
acrossaudiencemembercategories. WealsousedMR-QAP
matrix-based regression analyses in UCINET to analyze the
Playbouttermination
effectofsexandageclassesonthedyadicfrequencyofplayful
We used chi-square goodness of fit tests to compare the
behaviorsandsignals.
threeplayterminationcategories(Table4)andtestprediction
While these analyses might be less robust than others,
1 (third-party adult interference will end play more frequently
chi-square goodness of fit tests are valuable as they can use
thanotherformsoftermination). Resultsshowedastatistically
entire datasets to determine overall patterns (Reinhart et al.,
significant difference from the expected values (χ2(2)=53.52,
2010). We used chi-squared analyses to investigate general
P=0.001),indicatingthatterminationoccurredmorefrequently
patternsinTibetanmacaqueplay. However, asotherauthors
duetonon-playfulbehaviors(n=74)andwithdrawal(n=94)than
deviatefrominvestigationsofgeneralpatterns,morecomplex
tothird-partyadultinterference(n=16). Therefore,prediction1
analyseswouldbepreferabletoaccountforthewidevariation
wasnotsupported.
in assumptions that are violated by play-typical data (e.g.,
GLMM). Playsignals
Intotal,415playsignalsinplayfulinteractionswerecoded.The
RESULTS
averagenumberofplaysignalsseenincompletedplaybouts
Intotal,werecordedandanalyzed283dyadic(=2individuals) (n=94) was 1.6 play signals per bout. We used chi-square
andpolyadic(≥2individuals)playbouts,with136observations goodness of fit tests to compare the total frequency of play
of the start of play, 183 observations of the termination of bouts initiated by either a play behavior (Table 2) or a play
play, and94observationsofacompleteplaybout(wherethe signal (Table 3). Results showed a statistically significant
start and termination of play were clearly marked). In the 94 differencefromtheexpectedvalues,andthusprediction2was
completed play bouts observed, average length was 64.7 s, not supported (χ2(1)=45.88, P=0.001): play bouts were most
with a range of 1 to 585 s. The number of players present frequentlyinitiatedbyplaybehaviors(n=108)ratherthanplay
in a play bout ranged from 1 to 5, and all 22 juveniles were signals (n=28) (an unequal distribution across bouts). In the
observedtoengageinplayatleastonce. playboutsobserved(n=283),ninecandidateplaysignalswere
recorded,includingcrouch-and-stare(n=41),dangle-and-stare
Distributionofplayacrossindividuals (n=21),gamboling(n=3),hide-and-peek(n=1),look-back(n=1),
Only positively identified individuals were included in the playface(n=263),roll-onto-back-and-stare(n=19),playthreat
analyses (n=19). During play bouts, 16 juveniles exhibited (n=17), and slap-and-play face (n=49) (Table 5). Six of the
both play behaviors and signals during bouts. We seven candidate body signals observed in rhesus macaques
used chi-square goodness of fit tests to investigate the (Yanagi & Berman, 2014a) were also observed in Tibetan
distribution of individual engagement in play behaviors and macaques (crouch-and-stare, dangle-and-stare, gamboling,
signals. Play behaviors were differentially (as opposed to hide-and-peek, look-back, and roll-onto-back-and-stare). Two
equally) and significantly distributed across individuals (n=19; additional candidate signals were also observed (play threat
χ2(18)=4 016.06, P=0.001). Each juvenile engaged in playful andslap-and-playface).
behaviors between 4 and 589 times (125.35±169.58). Play We compared the frequency of play signals observed for
signaling was also significantly and differentially (as opposed zero (n=14), one (n=137), two (n=159), three (n=86), four
toequally)distributedacrossindividuals(n=19;χ2(15)=561.52, (n=16),andfiveaudiencemembers(n=3)andpredictedthatas
P=0.001). Eachjuvenileexhibitedplaysignalsbetween1and thenumberofaudiencemembersincreased,thefrequencyof
101times(25.56±30.93).Theseresultsindicatewidevariation playsignalswouldalsoincrease(prediction3;Table5).Results
in the frequency and use of playful behaviors and signals showed a significant statistical difference from the expected
278 www.zoores.ac.cn
values (χ2(5)=335.46, P=0.001); however, the Spearman’s weidentifiedwhenplaysignalswereusedbyacurrentplayer
rankcorrelationbetweenfrequencyofplaysignalsandnumber as a new member joined or a member withdrew from a
ofaudiencememberswasnotsignificant(r(4)=–0.371,P>0.05; bout.Resultsshowedasignificantdeviationfromtheexpected
Figure 1). Thus, these results suggest the trend between values (χ2(1)=6.025, P=0.001), and most players did not
play signals and audience members was not linear, but the use a play signal when a new member joined the bout (no
frequencyofplaysignalsacrossaudiencemembercategories signal=230, signal=26)or when anexisting memberwithdrew
wasdistributednon-randomly.Toexaminetheseresultsfurther, (nosignal=101,signal=24).
Table5Playsignalsobservedforeachaudiencemembercategory
Audience Play Dangle- Crouch- Hide- Look- Roll-onto-back- Play Slap-and- Total
Gamboling
number face and-stare and-stare and-peek back and-stare threat playface (n)
Zero 0 1 8 0 0 0 5 0 0 14
One 84 11 18 1 1 1 7 7 7 137
Two 104 6 11 1 0 0 4 7 26 159
Three 61 3 3 1 0 0 2 1 15 86
Four 11 0 1 0 0 0 1 2 1 16
Five 3 0 0 0 0 0 0 0 0 3
Total(n) 263 21 41 3 1 1 19 17 49 415
We used Spearman’s rank correlation to test prediction 4, as aggressive interactions. In despotic species such as
that play duration will be correlated with the rate of observed Tibetan macaques, observers of play may interpret a friendly
play signals. Results showed a strongly significant positive exchange as an aggressive one if it does not contain clear
correlationbetweentheobservedrateofplaysignalsandbout andfrequentplaysignals,andconsequentlymayterminateor
duration (Spearman’s rank correlation: r(5)=0.991, P=0.001; disrupt the play bout. However, our results did not support
Figure 2) and the average number of play signals and bout this prediction. In fact, play termination in juvenile Tibetan
duration (Spearman’s rank correlation: r(5)=0.964, P=0.001; macaquesusuallyoccurredbecauseindividualswithdrewfrom
Figure 3), thus indicating that as the length of a play bout the bout or engaged in non-play behaviors. We observed
increased, the average number and rate of play signals also only 16 cases in which other monkeys terminated the playful
increased. interaction:onecasebyalow-rankedadultmaleandonecase
byalow-rankedadultfemale,twocasesbyamid-rankedmale
DISCUSSION
andfivecasesbyamid-rankedadultfemale,threecasesbya
We examined the behaviors and candidate signals used in high-rankedadultmaleandtwocasesbyahigh-rankedadult
juvenile Tibetan macaque play bouts to characterize the play female, and two cases by a young adult female. We have
style of this species. Yanagi & Berman (2014b) found insufficient data to draw conclusions regarding the identities
that juvenile rhesus macaques use play signals in selective of the individuals who terminated these play bouts, but our
ways, as signals were non-randomly associated with various anecdotalevidencedoesnotfollowourpredictionbothinterms
subsequent play behaviors, and further hypothesized that oftheoverallnumberofthird-partyterminationsortheidentities
signalsmaybenecessarytoreinforceandclarifyplayfulintent. of the individuals who terminated the bouts. It is possible
Despotic macaques may use play signals more frequently to that juvenile macaques avoid areas occupied by adults to
emphasizetheaffiliative,ratherthanaggressive,natureoftheir directly manage the end of play themselves and avoid adult
behaviors. OurstudyshowedthatjuvenileTibetanmacaques interference(Selfetal.,2013).Additionally,althoughprediction
used similar play signals as rhesus macaques, but because 1 was not supported, due to their despotic dominance style
these behaviors did not frequently precede the beginning of and based on the Burghardt (2005) criteria for play, young
a play bout, their use may reinforce and clarify playful intent macaquesmayavoidadultstomaintainplayinarelaxedfield.
ratherthansignaltheinitiationofabout. However, further comparative research is needed to test the
Bermanetal.(2004)hypothesizedthatduetotheirdespotic hypothesis that social organization in all macaque species
nature,Tibetanmacaqueadultswouldinterferewithplaybouts (including Grades 2 and 3) may influence play style (but see
perceivedbythirdpartiesasaggressive.Manybehaviorsused Reinhartetal.,2010), andthereforeplayterminationbyadult
in play, such as bite, wrestle, and chase, are also used in interference.
aggressive contexts and could potentially be misinterpreted
ZoologicalResearch39(4):272–283,2018 279
180
180 signalinginjuvenileTibetanmacaquesmaybeusedsimilarly
160
160 159 tosignalinginjuvenilerhesusmacaques,inwhichplaysignals
140 159 areusedtoclarify,reinforce,andprolongaplayboutbetween
140 137
n) 120 137 partners (Yanagi & Berman, 2014b). Furthermore, our data
Frequency of play signals (n)Frequency of play signals(111468024680000000000 86 86 (smmdfaphrceoraoeemrwwedn(biecnsedtf=iirrgoos2annm6aa33npl;st;dohSseTonsuascuipebbcmpllueerblreere5smitnrr;uegeolFtnnfsidwgt.pauliratIbrhtyyeeatFsopw1iinpgg)e.eenueaarSneorlsesrtSvhgtte1hweer)anaotmneluiracnoamoudrtnedeibvcideetildhurninuascoanieaoflsnobmastuohuesucedmetari,enbppwnellbicaatreehsyy
2200 signals(n=152),regardlessofaudiencenumber.Thisindicates
00 Z1e4r1o4 One Two Three F1o6ur 16 Fi3ve 3 the salient nature of the play face signal when there is a
Zero One Two Three Four Five receiverpresent(Pellis&Pellis,1996;vanHooff,1967)orwhen
Number of audience members (n)
Number of audience members (n) acombativeplaybehavior,suchasplayslap,mayescalateto
FFiiggurue r1e Fr1eqFuernecqy uofe pnlacyysigonaflsp wlaityh dsififgernenat lasudwienitche mdeimffbeerrse ntaudience
Figure 1 Frequency of playsignals with different audience members aggression(Palagietal.,2007).Thiswasfurthersupportedby
members
the lack of play face observed in the zero-audience member
category (when no other group member was in proximity
12
to the initiator). Therefore, play face may be an important
12
(n)10 communicativetoolinpolyadicplaywhenaplayerisnearthe
Average number ofplaysignalsAverage number of play signals (n)10246824680 1sotpt&zaooee9tllalhrPn6ocytoehd7elft-rauhee)lasl.rleiruis.ifirpndy,nHTlcitap1eeoaphyr9nwntlioeaes9ctxeryig6eosirvmo)enew.mrst,irihth,eueyaMeeslpmsttmnool(sabirnstuetyte=hehcgor4elefagvvac0neeebcad1rssoeb,ty)teu,nest(mgthaPatuorenmaheasrdyalyteilohcittsdcb(ehspncerei&lu=noatlhar1yfaraPa4ectfghnea)knveelcacwlgonieersefabei,enomsorotae1byufamlr9styasoes9uictfgirb6ecghvcnhe;dnaeoaandaalnvloilgsatnpwessengalixehagt(syroiHnsPniwtagfoeahatlniolnhnacltaifodegnesfl,
0 60 120 180 240 300 301+
Bout length (s) may be an artifact of this sampling. Additionally, the frequent
0 occurrence of play face may be an involuntary artifact of the
0 60 120 180 240 300 301+
sender’s enjoyment of the bout rather than a message for
Bout length (s)
31 players(Spijkermanetal.,1996).
Figure2Averagenumberofobservedplaysignalsperbout Onlythreeplaysignalswereobservedinthezero-audience
length membercategory: (1)crouch-and-stare,(2)dangle-and-stare,
Figure 2 Average number of observed playsignals per bout length 31a nd(3)roll-onto-back-and-stare.Thismayindicatetheneedto
usecomplexbodyandfacialsignalstoattractplayerstobegin
0.2
a bout, rather than a face-only signal. For example, juvenile
0.18 chimpanzees often use attention-getting gestures when a play
0.16 partnerdoesnotseethesignalsender’splayface(Tomaselloet
nals per 60 s00..1124 aothlf.e,tw1so9e8no9dr)e.mrI’snormteheisssigwsnaaagyl,esa.mpOalauyyrbrseeigsnnuealtclsethssasuatpripnyovtrootlvtaehmsispthslipefyeccoourmlraebtiiionnnfao,triocanes
play sig00.0.81 jduivveenrsileebTeibheatvainoramlarceapqeurteosireustoedinmdiuclatitpelethpelairywsiilglinnganlsesfrsomtotphleaiyr
Rate of 0.06 with conspecifics. However, a larger sample of zero-audience
memberplayboutsisneededforfurtherinvestigation.
0.04
Additionally, across all audience member categories, the
0.02
leg-peek signal (see Table 3) was never observed. Yanagi
0 & Berman (2014b) found that in rhesus macaques, the
0 60 120 180 240 300 301+
Bout length (s) leg-peek was associated with play initiated by the receiver
and may have served as a play invitation. However, this
Figure3Rateofobservedplaysignalsper60sacrossbout
signal was not present in Tibetan macaque play, indicating
Figure 3 Rate of observed play signals per 60 s across bout length
length that leg-peek may be a species-specific signal. Similarly, two
candidateplaysignalswereobservedintheTibetanmacaque
repertoire that were not observed in rhesus macaques: play
We found that more play bouts began with play behaviors
threat (Supplementary Figure S2) and slap-and-play face
thanplaysignals(notsupportingprediction2). Therefore,play
280 www.zoores.ac.cn
32
(Supplementary Figure S3). Adult Tibetan macaques use and in various contexts, as they were observed before, during,
threat behavior as part of an aggressive interaction, and andwhenwithdrawingfromplay(Pellisetal.,2011).
it is characterized by an open mouth gesture and another Finally, we examined the length of play bouts in relation to
body movement, such as a ground slap, raised eyebrow, or thenumberofplaysignalsused(prediction4;Figure2;Figure
lunge(Bermanetal.,2004). Therefore,theplaythreatsignal, 3). Spearman’s rank correlation showed a strong statistically
observedduringplaybouts, maypotentiallybeanincomplete significant correlation, thus supporting this prediction and
adult threat behavior, with the absence of the open mouth indicating the likely importance of play signals in sustaining
facial expression. Play threat may enable juvenile macaques aplaybout. Previousliteraturehasshownthatplayboutstend
to practice components of adult behavior within the context tobelongerwhenplayersusetheplayface(Waller&Dunbar,
of play (Martin & Caro, 1985). However, further research is 2005), playful facial expressions punctuate bouts rather than
needed to confirm that the candidate play signals observed initiatethem(Palagietal.,2007),thirdpartiesjointheplaybout
in Tibetan macaque juveniles do not occur under any other more often when the play face signal is used, and long play
contexts. Although the characterization of Tibetan macaque boutsaretypicallymoreintenseandcontainmoreplayfaces,
play signaling differs from that of rhesus macaques, there especially when ambiguous behaviors are involved (such as
does appear to be some cross-species similarity in both wrestle and gnaw) (Spijkerman et al., 1996). This increased
play behavior and signaling repertoires. The similarities and signalingmaybecriticalformaintainingplayfulinteraction, as
differences in their play style may reflect social organization additional evidence indicates that short play bouts are often
(Palagi,2006);however,morecomparativeresearchisneeded. marked by a misinterpretation of signals, thus halting play.
Relative to audience members, we observed the OurstudydemonstratedthatcandidateplaysignalsinTibetan
combination of slap (a play behavior) and play face (a play macaquesmaybeusedinsimilarways, withthelongestplay
signal) more than other play signals, such as gamboling, boutscontainingthemostplaysignals. However,furtherstudy
hide-and-peek, and look-back (Figure 1). It is possible that isneededtoexaminethecausalrelationshipbetweenplaybout
the playful intention of a slap behavior needs to be clarified lengthandthefrequencyanddistributionofplaysignals.
asplaybecauseofitsassociationwithaggression(Burghardt,
1999;Pellis&Pellis,1996). Inthisway,theslapbehaviorand CONCLUSIONS
play face signal would contradict each other and, therefore,
mightincreasethelikelihoodofthereceiverunderstandingthe Juvenile Tibetan macaques maintained playful interactions
situationasnon-threatening. using multiple candidate play signals, which combined body
Although we expected that more play signals would be andfacialgestures,tobeginplay,encouragethecontinuationof
observed in polyadic play bouts (at least one actor and two play,andendplay.Acrossallaudiencemembernumbers,play
audience members) (Spijkerman et al., 1996), we did not face was the most frequently observed play signal, possibly
find support for this prediction. Our results indicated that two indicating its salient and general nature. Tibetan macaque
audiencemembers(threeplayersintotal)includedthelargest juveniles utilized play behaviors and signals similar to rhesus
numberofplaysignalsemittedforthisboutcomposition. The macaques;however,thedifferencesobservedintheirplaystyle
playsignalsobservedinplaygroupslargerthanthreemembers andsignalvarietymaybeinfluencedbythedominancestyleof
werelessfrequent,andthenumberofplaysignalsusedwithin Tibetanmacaques.
larger group compositions declined as more members were
added. Thisresultimpliesapossiblethresholdforthesaliency COMPETINGINTERESTS
of play signals past a certain audience member number. It
is possible that play bouts with more players increase the Theauthorsdeclarethattheyhavenocompetinginterests.
complexityofthebout,makingthemhardertomanage(Bekoff,
1972). Furthermore, the play signal message may lose
AUTHORS’CONTRIBUTIONS
salienceasthecomplexityandsizeoftheplaygroupincrease
beyond three players. This breakdown of communication
K.R.W., J.A.M., and L.K.S. designed the study. L.K.S. (P.I.) and R.W.S.
may be more readily observed in despotic macaques due to
(co-P.I.)acquiredfundingthatpartiallysupportedthisresearch(NSF-OISE
their strict social organization and therefore more risky and
1065589). K.R.W.andR.S.Wcollecteddata, andJ.H.L.superviseddata
uncertainsocialinteractions. Itisalsoreasonabletoconclude
collectioninthefield.K.R.W.andJ.A.F.performedstatisticalanalysis,under
that play bouts with fewer members reinforce affiliative bonds
the supervision of J.A.M, L.K.S., and L.S. K.R.W. and J.A.M. wrote the
betweengroupmembers,whereaslargerplaygroupsmaybe
manuscriptwiththeotherauthors’input. Allauthorsreadandapprovedthe
used to assess individuals’ physical strengths (Pellis & Pellis,
finalmanuscript.
1996).Therefore,signalingmaybecrucialinasmallplaygroup
toreaffirmthesocialcontext: affiliationratherthanaggression.
ACKNOWLEDGEMENTS
Ourresultsalsoshowedthatplaysignalswerelesslikelytobe
emittedwhennewaudiencememberswereaddedtoaboutor
We thank the Huangshan Garden District Bureau staff for permission to
whenaplayerleftabout. Thisindicatesthatwhenplaysignals
conductresearchatthefieldsite,andXiWangandtheChenfamilyfortheir
areusedbyjuvenileTibetanmacaques,theyareusedgenerally
operationalsupportandencouragementinthefield.
ZoologicalResearch39(4):272–283,2018 281