Social functions of relaxed open-mouth display in golden snub-nosed monkeys (Rhinopithecus roxellana)

2019·2.1 MB·

by  Zhang, You-Ji

ZOOLOGICAL RESEARCH
Social functions of relaxed open-mouth display in
golden snub-nosed monkeys (Rhinopithecus roxellana)
You-JiZhang1,2,#,Yi-XinChen1,#,Hao-ChunChen1,YuanChen1,HuiYao3,Wan-JiYang1,3,Xiang-DongRuan4,
Zuo-FuXiang1,2,*
1InstituteofEvolutionaryEcologyandConservationBiology,CentralSouthUniversityofForestry&Technology,ChangshaHunan410004,
China
2CollegeofLifeScienceandTechnology,CentralSouthUniversityofForestryandTechnology,ChangshaHunan410004,China
3ShennongjiaNationalPark,ShennongjiaForestDistrict,ShennongjiaHubei442411,China
4NationalForestInventoryandDesignInstitute,Beijing100714,China
ABSTRACT reassuranceincoordinatingsocialinteractionswithin
Relaxedopen-mouthdisplayservesimportantsocial OMUsingoldensnub-nosedmonkeys.
functions in relation to submission, reconciliation,
Keywords: Golden snub-nosed monkey; Open-
affiliationandreassuranceamongnon-humanprimate mouth; Submission; Reconciliation; Affiliation;
societies; however, quantitative evidence on this Reassurance
behaviorremainsinsufficientamongmulti-levelsocial
INTRODUCTION
groups. FromJulytoNovember2016, weexamined
Open-mouth display is a common social behavior in
four potential functions of the relaxed open-mouth
non-human primates. It comprises individuals opening their
display during pairwise, intra-unit social interactions
mouths and presenting their teeth or canines and can be
among 18 free-ranging adult and sub-adult golden
associated with different body postures and behaviors in
snub-nosedmonkeys(Rhinopithecusroxellana)who either hostile or relaxed scenarios (Altmann, 1962; Hinde
belonged to three one-male, multi-female units & Rowell, 1962; Yang et al., 2013). There are diverse
(OMU) at Dalongtan, Shennongjia National Park, patternsandfunctionsofopen-mouthdisplayamongprimates.
In hostile scenarios, open-mouth displays are aggressive.
China. Results showed that: compared with no
As observed in Macaca mulatta and Macaca arctoides,
relaxed open-mouth display, (1) the occurrence of
open-mouthdisplaybydominantindividualsinvolvestheslight
displacement by a dominant individual approaching opening of mouths and presentation of mandibles, followed
a subordinate was lower and the distance of by teeth chattering, pulling back of lips and orienting their
the subordinate to the approaching dominant was heads towards subordinates while making threatening calls;
shorter when the subordinate showed open-mouth if subordinates do not respond submissively, the aggression
can escalate to ritualized fighting or physical attack, resulting
display; (2) relaxed open-mouth display reduced
in subordinate displacement (Altmann, 1962; Hinde & Rowell,
the probability of continued attack for victims of
1962;Renetal.,1990a).
aggression and allowed victims to achieve closer
proximity to the aggressor during post-conflict
periods;(3)relaxedopen-mouthdisplaybydominant Received: 08April2018;Accepted: 30July2018;Online: 13August
individuals allowed them to achieve closer proximity 2018
to subordinates; and (4) the exchange of relaxed Foundationitems: ThisstudywassupportedbytheNationalNatural
open-mouth display had a greater impact on the Science Foundation of China (31670397, 31870509) and Science
outcome of interactions than one individual alone FoundationoftheStateForestryAdministrationofChina
giving this signal. These findings suggest that #Authorscontributedequallytothiswork
relaxedopen-mouthdisplayservesimportantfunctions *Correspondingauthor,E-mail:[email protected]
regarding submission, reconciliation, affiliation and DOI:10.24272/j.issn.2095-8137.2018.043
SciencePress ZoologicalResearch40(2):113–120,2019 113
Inadditiontothefunctionsofaggressioninhostilescenarios, subordinate shows relaxed open-mouth display; and the risk
researchers have noted that relaxed open-mouth displays in of continued aggression by an aggressor should be reduced if
normal, calm or post-conflict periods are crucial in many the victim shows relaxed open-mouth display; (2) for affiliation,
primatespeciesforsubmission,reconciliationandreassurance thedistancefromthesubordinatetotheapproachingdominant
tocoordinatesocialinteractions,increasesocialtoleranceand individualshouldbeshorterwhenthesubordinateshowsrelaxed
maintaingroupstability(Aureli,1997;deWaal,1986;deWaal open-mouthdisplay;(3)forreconciliation,thedistancebetween
&Luttrell,1989;deWaal&Ren,1988). the aggressor and victim should be closer if the victim shows
Until now, only a handful of studies have quantitatively relaxedopen-mouthdisplay;and(4)forreassurance,adominant
testedfunctionalhypothesesofrelaxedopen-mouthdisplayin individualshouldbeabletoapproachasubordinatemoreclosely
behavioral interactions among non-human primate societies. whenshowingrelaxedopen-mouthdisplay.
For example, within social groups of Trachypithecus francoisi,
MATERIALSANDMETHODS
lower-ranked members exhibit submissive behavior when
being attacked by dominant individuals, including opening Studysiteandstudygroup
mouthsandshowingteeth,shakingheadsslightly,andkeeping WeconductedthestudyatDalongtan,ShennongjiaNationalPark,
the body and limbs slack, to ease tension and decrease the Hubei, China(N31◦29(cid:48)65(cid:48)(cid:48), E110◦17(cid:48)93(cid:48)(cid:48); 2170ma.s.l.). The
possibility of continuous attack (Wang, 2009). In groups of study site is comprised of highly seasonal deciduous broadleaf
Mandrillus sphinx, frequencies of relaxed open-mouth display andconiferforest.Themonthlyaveragetemperaturerangesfrom
and teeth chattering during post-conflict periods between two 17.11◦CinJulyto–3.51◦CinJanuary(Yaoetal.,2011).
individuals are significantly higher than during pre-conflict During the study period, the study group consisted of 76
periods, suggesting that relaxed open-mouth display may individualsbelongingtofiveOMUsandoneAMU.Reservestaff
have important reconciliatory effects (Bout & Thierry, 2005). havesuccessfullyhabituatedandprovisionedthisgroupsince
In groups of Macaca sylvanus, the exchange of relaxed 2006, making close observation and individual identification
open-mouth display (i.e., presented by both subordinate and possible(Yaoetal.,2011).Wewereabletoidentifyandname
dominant individuals) has greater impact than when one each individual based on distinct physical features of the body
individual alone displays the signal (Wiper & Semple, 2007). andface, e.g., bodysize, furcolor, shapeofnipplesinfemales,
Relaxedopen-mouthdisplaymayalsofunctionasreassurance, shape of granulomatous flanges on sides of upper lip in males,
a kind of affiliative signal exhibited by dominant individuals and body deformities. We named each OMU based on the
opening their mouths slightly and approaching subordinates male leader’s name (Xiang et al., 2014; Yao et al., 2011; Yu et
under normal, relaxed scenarios (van Hooff, 1967; Wiper & al., 2013). Reserve staff provisioned the monkeys twice daily
Semple, 2007), as observed in groups of Mandrillus sphinx (1130–1200hand1800–1830h,UTC+8)withlichen,pineseeds,
andMacacasylvanus(Bout&Thierry,2005;Wiper&Semple, apples, carrots, peaches and peanuts. When not provisioned,
2007). the monkeys ranged freely across an area with a radius of
The golden snub-nosed monkey (Rhinopithecus roxellana) approximately1km(Xiangetal.,2014). Tomaximizesampling
is endemic to China, inhabiting the Sichuan, Gansu, Shaanxi effortsduetothelimitedperiodandOMUscontaininginsufficient
and Hubei provinces (Guo et al., 2007; Yao et al., 2011). adults,wechose18adultsandsub-adultsasfocalindividuals
Thisspeciesischaracterizedbyamulti-levelsocietyconsisting (4–19yearsold)fromthethreeOMUswiththegreatestnumber
of several one-male, multi-female units (OMUs), at least one ofadultfemales(HH,XZ,andXB,Table1)andrecordedrelaxed
all male unit (AMU), and satellite solitary males forming a open-mouthdisplaysduringintra-unitsocialinteractions.
large and cohesive group (Qi et al., 2014). In addition to the
Datacollection
common function of aggression, researchers have suggested
Dominancerank
that relaxed open-mouth display in R. roxellana may also
Ourstudywasdividedintotwosuccessiveperiods. Inthefirst
functioninsubmission,reconciliation,affiliationorreassurance
period (22 July–31 August 2016) before systematic sampling,
during normal, calm or post-conflict periods (Li et al., 2006;
we used an “aggression-submission” index to calculate the
Ren et al., 1990b; Yan et al., 2006; Yang et al., 2013).
dominance rank of each individual within an OMU (Martin &
However,theseconclusionsareprimarilybasedonqualitative
Bateson,1993). Weobservedthestudygroupfromdistances
observations, with no current research providing quantitative
of 3–20 m from 0830 h to 1130 h and 1430 h to 1730 h
evidenceregardingthefunctionsofrelaxedopen-mouthdisplay
(UTC+8). Usingall-occurrencesampling(Altmann,1974), we
in golden snub-nosed monkeys during normal, relaxed or
recorded every incidence of “aggression-submission” as well
post-conflictperiods.
astheinitiators, recipients, andallsocialbehaviorsrelatedto
Here, we studied pairwise, relaxed open-mouth display conflict(e.g.,grasping,chasing,displacing,threatening,avoiding,
in a free-ranging group of R. roxellana and quantitatively crouching and fleeing) involving the 18 focal individuals. Due
tested four potential functional hypotheses–i.e., submission, to our focus on intra-OMU pairwise interactions and to avoid
reconciliation,affiliationandreassurance–duringnormal,relaxed biases from multi-individual alliances within or among OMUs,
andpost-conflictperiods. Wepredictedthat: (1)forsubmission, weonlyrecordedintra-OMUaggressive-submissivebehaviors
the occurrence of displacement by a dominant individual involvingtwoindividuals.
approaching a subordinate should be less frequent when the
114 www.zoores.ac.cn
Table1Aggressiveandsubmissivebehaviorsamplingnumberandrankofeachindividualinthreefocalunits
Aggressive Submissive
SocialUnit Individual Sex Age Sum Dominanceindex Rankingorder
behavior/acts behavior/acts
HH M Adult 37 9 46 0.94±0.03 1
HH2 F Adult 33 15 48 0.79±0.16 2
HHE F Adult 12 6 18 0.56±0.18 3
HH YY1 F Adult 10 5 15 0.48±0.20 4
DWB F Adult 4 3 7 0.36±0.20 5
TJ F Adult 14 2 16 0.32±0.13 6
AL F Sub-adult 3 0 3 0.06±0.04 7
XZ M Adult 38 24 62 0.92±0.04 1
XB2 F Adult 36 18 54 0.80±0.15 2
XE F Adult 26 12 38 0.50±0.19 3
XZ
YB F Adult 24 9 33 0.41±0.15 4
XH F Adult 12 8 20 0.29±0.16 5
SB F Sub-adult 7 0 7 0.08±0.03 6
XB M Adult 23 13 36 0.91±0.03 1
GG F Adult 17 5 22 0.67±0.20 2
XB LN F Adult 23 5 28 0.50±0.20 3
SS F Adult 15 4 19 0.34±0.22 4
YY2 F Adult 3 1 4 0.08±0.03 5
Sum 337 139 476
M:Male;F:Female.
We defined an individual of higher rank to be dominant in contact(Wiper&Semple,2007). Wesimultaneouslyrecorded
eachpairwisesocialinteraction(involvingtwoindividualsonly) theidentitiesofthetwoindividualswhoapproachedeachother,
and the lower-ranked individual to be subordinate. Similarly, whether displacement, aggression or continued aggression
whenaggressionoccurred,wedefinedtheonewhothreatened occurred, the presence or absence of relaxed open-mouth
or attacked another individual to be the aggressor and the display,andtheclosestdistancebetweenthetwoindividuals.
other party to be the victim. In most cases, aggressors were We defined relaxed open-mouth display as an instance
dominant,andvictimsweresubordinate(Renetal.,1990b). when an individual slightly opened mouth without presenting
During the study period, we also provisioned the 18 focal canines, with an associated relaxation of limbs, head, neck
individuals with peanuts on four occasions per month to andshoulders(Renetal.,1990b)(Figure1A,B).Furthermore,
ascertain whether intra-OMU hierarchy remaining unchanged, during such action, the individual could approach another
i.e.,the“nuttest”(Prud’Homme,1991;Wiper&Semple,2007). OMUmemberwithonlyslightcommunicativecallsratherthan
In the test, we positioned peanuts, a highly favored food threatening sounds (Li et al., 1993). We considered both
item, at a point equidistant from two individuals to invoke a individualsexhibitingtheseactionsasan“exchangeofrelaxed
dominance-basedinteractionandassumedtheindividualwho open-mouthdisplay”(Wiper&Semple,2007).
approachedandatethepeanuttobethedominantofthetwo
Additionally,wedefinedtherelatedbehavioralpatternsand
(Prud’Homme,1991;Wiper&Semple,2007).Tominimizebias,
hypothesizedfunctionsasfollows:
werepeatedthenuttestthreetimesoneachoccasionwhenwe
Aggression: aggressorsthreatenedandattackedvictimsby
wereunsureoftheintra-OMUhierarchy.
openingtheirmouthsaggressivelyandstaring,whiletightening
Relaxed open-mouth display and related behavior their head, neck, shoulder and limb muscles and initiating
definitions warning calls (Figure 2A, B). Ritualized fighting or physical
Basedonthedominancerankdataobtainedinthefirstperiod, attackcouldoccurifvictimsdidnotrespondsubmissively(Cui
duringthesecondperiod(1September–4November2016)we etal.,2014;Lietal.,2013).
used focal animal sampling (Altmann, 1974) to record relaxed Post-conflict period: a period lasting up to 10 min after
open-mouthdisplaysofeachfocalindividualfor30minbetween aggressorscompletelyceasedthreateningorattackingvictims.
0830–1130hand1430–1730hperday(UTC+8). Duringthisperiod,relaxedopen-mouthdisplayandsubmissive
Focal animal sampling began when one individual behaviors, especially exhibited by victims, eased tension and
approached the focal individual to within 5 m or the focal individuals gradually returned to a relaxed or normal status
individualmovedtowardanotherindividualwithin5mwitheye (Renetal.,1991).
ZoologicalResearch40(2):113–120,2019 115
1991).Thefunctionofreconciliationbehavioristhoughttobea
recoverymechanismofthesocialrelationshipbetweenthetwo
opponents(deWaal&vanRoosmalen,1979).
Reassurance: dominant individuals actively and firstly
openedtheirmouthswithoutpresentingcaninestoreducethe
risk of aggression perceived by subordinates in post-conflict
or relaxed periods. Reassurance is a form of affiliation but is
considered separately as the dominant individual, rather than
thesubordinate,isthekeysignaler(Wiper&Semple,2007).
Finally, relaxed open-mouth display in this study
Figure 1 Relaxed open-mouth display in golden snub-nosed monkeys (Rhinopithecus roxellana)
(Figure1A,B)wasquitedifferentfrom“aggressiveopen-mouth
Figure 1 RelaxFeidg uopreen1-mRoeultahx deidspolapye nin- mgooludtehn dsinsupbl-anyosiend gmooldnekneyss n(uRbh-innoopsiethdecus roxellana)
during normal, remlaoxnekde oyrs p(oRsth-cinoonfpliitcht epceurisodrso x ellana)duringnormal,relaxedor display” in behavioral patterns (Figure 2A, B), although the
during normal, preolsaxt-ecdo onrfl picotstp-ceorinofdlisct periods latterisubiquitousamongRhinopithecusspecies(R.roxellana:
Canines are not presented. A: Male; B: Female.
Caninesarenotpresented.A:Male;B:Female.PhotobyYou-JiZhang. Renetal.,1991;Yangetal.,2013;R.bieti: Lietal.,2013;R.
Canines are not presented. A: Male; B: Female.
brelichi:Cuietal.,2014).

Dataanalysis
Analysisofdominancerank
We adopted the dominance index to explore the intra-OMU
dominance rank of the 18 focal individuals using four steps
(Renetal.,1990c;Zumpe&Michael,1986).
(1)Percentageofaggressivebehaviorsgiven: foreachpair
ofindividuals,wecalculatedthepercentageofthetotalnumber
ofaggressivebehaviorsgivenbyeachparticipanttotheother.
(2) Percentage of submissive behaviors received: for each
Figure 2 AggressFiivgeu orpee2n-Amgogurtehs dsiisvpelaoyp ienn g-molodeunth snduisbp-nlaoyseidn mgoolndkeenyss n(Ruhbi-nnoopsitehdecus roxellana)
pairofindividuals,wecalculatedthepercentageofsubmissive
Figure 2 Aggremssoivnek oepyesn(-Rmhoiuntoh pdiitshpelacyu sinr gooxledlelann san)udb-unroinsegdh moosntikleeyssc (eRnhainrioopsithecus roxellana)
during hostile scenarios. behaviorsreceivedbyeachparticipantfromtheother.
Cdaunrininegs haroes tpilree sseCcneatnneiadnre,i osfasac.r iea pl reexspernetessdi,ofancsi aalnedx pbroedssyi opnossatunrdebso adryep aogsgturreesssiavree.a Agg: rMesaslieve; .B: Female(3. ) Percentageofaggressiongivenandsubmissionreceived
Canines are preAs:eMntaelde,; Bfa:cFieaml eaxlep.rPeshsoitoonbsy aYnodu -bJoiZdhya pnogs.tures are aggressive. A: Male; B: Fepmearlep. a ir: we combined the percentage scores of aggression
givenandsubmissionreceivedforeachindividualinthepair.

Continued aggression: aggressors continued to threaten (4) Dominance index: we evaluated the dominance index
or attack victims after the initial aggression occurred, even if by averaging, for each individual, the percentage scores
victims exhibited relaxed open-mouth display and submissive of aggression given and submission received with all other
behaviors. Continued aggression could occur subsequently individualsinthegroup.
after the initial aggression or could erupt anytime within 10 Finally,weproducedthedominancerankbysequencingthe
min of the post-conflict period (Ren et al., 1991). It could be intra-OMUdominanceindexvaluesfromhightolow.
relentlessaggressivebehaviorortheescalationofaggression
fromthreattoritualizedfight,evenphysicalattack. Analysisofrelaxedopen-mouthdisplay
Displacement: a higher-ranking individual displaced a We divided all behavioral data into the following categories:
lower-ranking individual to occupy a superior position (such “absence of relaxed open-mouth display” vs. “presence of
as a cool, warm or feeding place). During displacement, relaxed open-mouth display” and “single individual showing
the subordinate typically showed evasive behavior and open-mouthdisplay”vs.“bothindividualsshowingopen-mouth
surrenderedafoodresourceorfavoredsitewhenthedominant display”. We then respectively summed the occurrences
individualapproached(Yanetal.,2006). of displacement and continued aggression, and distances
Submission: a series of behaviors performed by victims to betweendominantindividualsandsubordinatesoraggressors
preventcontinuedaggression, includingopeningtheirmouths andvictims.
and showing teeth, slightly shaking their heads, and keeping We adopted the Chi-square test to detect differences in
Figure 3 Closest distance achieved by a subordinate approaching a dominant individual
theirbodyandlimbsslack(Lietal.,2013;Wang,2009). the occurrences of displacement and continued aggression
Figure 3 Closest distance achieved by a subordinate approaching a dominant individual
Affiliation: friendly contact between individuals to maintain under different relaxed open-mouth display patterns. We
group balance (Ren et al., 1990b). Subordinates slightly used one-way analysis of variance (ANOVA) for overall
opened their mouths or both subordinates and dominants comparison followed by t-tests (SPSS v17.0) to identify
exchanged relaxed open-mouth display to attain a closer differences in distances between subordinates, dominants,
distanceandeasetensionintheOMU. and/or aggressors and victims. Each sample showed normal
Reconciliation: any affiliative contact between former distribution. Statistical tests were two-tailed, and significance
opponents within 10 min after a conflict ceased (Ren et al., wassetat0.05.
116 www.zoores.ac.cn
Ethicalstatement We recorded three different relaxed open-mouth display
Prior to conducting this study, we obtained approval from the patternswhensubordinatesapproacheddominantindividuals,
Shennongjia National Park and the Institutional Animal Care i.e.,subordinatesdidnotshowopen-mouthdisplay(40times),
andUseCommitteeofCentralSouthUniversityofForestryand only subordinates showed open-mouth display (31 times)
Technology. and both subordinates and dominants showed open-mouth
display (28 times). The average minimum distance achieved
RESULTS
by subordinates approaching dominant individuals without
Dominancerank becoming the target of aggression is shown in Figure 3.
We observed aggressive behavior 337 times and submissive Relaxed open-mouth display had a significant effect on
behavior 139 times. Based on our calculation of dominance distance (F=37.062, P<0.001). Subordinates were able to
index, we ranked the 18 focal individuals within their OMUs get closer to dominant individuals if they exhibited relaxed
as follows: HH unit, HH>HH >HHE>YY >DWB>TJ>AL; XZ open-mouth display than if they did not (t=4.796, P<0.001).
2 2
unit, XZ>XB >XE>YB>XH>SB; XB unit, XB>GG>LN>SS>YY Furthermore, exchange of relaxed open-mouth display from
2
(Table1).Theintra-OMUhierarchyremainedstablethroughout bothparticipantsfacilitatedtheclosestdistancesbetweenthem
the entire study period (22 July–4 November 2016) bFaisgeudre o1n Relaxe(dt= o5p.0e6n-8m,Pou<t0h .0d0is1p)l.ay in golden snub-nosed monkeys (Rhinopithecus roxellana)
theresultsfromtherandomnuttests.
during normal, relaxed or post-conflict periods
Relaxedopen-mouthdisplay Table3Timesofcontinuedaggression
Canines are not presented. A: Male; B: Female.
Weobservedrelaxedopen-mouthdisplay212timesoutof322
Occurrence No. Statisticaltests
totalapproacheswithintheOMUs. Theoccurrenceofrelaxed
ofcontinued continued (Chi-square
open-mouth display was related with displacement 29 times
aggression(n) aggression(n) test)
(13.68%, n=212), with aggression 24 times (11.32%, n=212),
with friendliness 59 times (27.83%, n=212), with post-conflict Neithervictim
period 53 times (25%, n=212) and with reassurance 47 noraggressor
times (22.17%, n=212). We obtained 154 h of observation showedrelaxed 10 1
on the focal group, and the average occurrence of relaxed open-mouth
χ2=14.368,
open-mouth display for the 18 focal individuals was 1.38 display
times/h. The displacement occurrence of subordinates by Victimsalone P<0.001
approaching dominant individuals is shown in Table 2. There showedrelaxed
4 20
was a higher risk of being displaced by a dominant individual open-mouth
if the subordinate did not exhibit relaxed open-mouthFidgiusrpel a2y Aggressive odpisepnla-my*outh display in golden snub-nosed monkeys (Rhinopithecus roxellana)
(χ2=25.259,P<0.001)(Table2).
during hostile sc*e:nTahreiores. w ereno“Aggressorsaloneexhibitedrelaxedopen-mouth
Table2DisplacementoccurrenceofsubordinatesbyappCroaancihneinsg are presdeisnptelady, ”f.acial expressions and body postures are aggressive. A: Male; B: Female.
dominantindividuals

Occurrenceof No. Statistical
displacement displacement tests(Chi-
event(n) event(n) squaretest)
Neitherdominant
norsubordinate
21 2
showedrelaxed
open-mouthdisplay χ2=25.259,
Subordinates P<0.001
aloneshowed
5 24
relaxedopen-
mouthdisplay*
*:Therewereno“Dominantsaloneexhibitedrelaxedopen-mouth
display”.
Table 3 shows the occurrence of continued aggression
during the post-conflict period. The occurrence of continued
Figure 3 ClosestF digisutarence3 achCileovseeds bty ad issutbaonrcdeinaatec hapiepvroeadchibnyg aa domsuinbaonrtd iinndaitveidual
aggression was lower when victims alone exhibited relaxed
approachingadominantindividual(n=99)
open-mouthdisplaytowardsaggressors(χ2=14.368,P<0.001)
(Table3). ***:P<0.001.
ZoologicalResearch40(2):113–120,2019 117
Afteraggressiveeventsceased,werecordedthreedifferent DISCUSSION
relaxedopen-mouthdisplaypatterns,i.e.,victimsdidnotshow
We explored four hypotheses related to relaxed open-mouth
open-mouth display (11 times), victims showed open-mouth
displaywithintheOMUsoffree-rangingR.roxellana. Results
display toward aggressors (24 times) and both participants
suggestedthatrelaxedopen-mouthdisplayservedfoursocial
showedopen-mouthdisplay(29times). Relaxedopen-mouth
functions in R. roxellana societies: that is, submission,
display had a significant effect on distance (F=34.907,
reconciliation, affiliation and reassurance. Furthermore, an
P<0.001). Byexhibitingarelaxedopen-mouthdisplay,victims
exchange of relaxed open-mouth display facilitated more
were able to get closer to aggressors (t=3.759, P<0.01), and
significant outcomes than when one individual exhibited the
exchange of relaxed open-mouth display allowed victims and
behavioralone.
aggressorstogetmuchcloserthanwhenonlyvictimsexhibited
n=99. ***: P<0t.h0e01b; e*h*:a Pvi<o0r.0a1lo. ne(t=2.828,P<0.01)(Figure4). In our study group, relaxed open-mouth display usually
functionedasasignofsubmission. Forsubordinates,relaxed
open-mouth display significantly reduced the probability of
being displaced when dominant individuals approached
(Table2). Forvictims,relaxedopen-mouthdisplaysignificantly
reduced the occurrence of continued aggression (Table 3).
Theseoutcomesaresimilartothosereportedinpreviousstudy
onR.roxellanapopulationsintheQinlingMountainsofChina,
n=99. ***: P<0.001; **: P<0.01.
whereadultfemalesandjuvenileswereobservedtoopentheir

mouthstoexhibitsubmission,preventaggressionandmaintain
OMUstability(Yangetal.,2013).
Relaxed open-mouth display also served as a clear signal
of reconciliation as aggression was unlikely to continue while
aggressors and victims could reengage in social interactions
in close proximity (Figure 4). These results are in agreement
with those reported from a captive group of R. roxellana
(Ren et al., 1991), as well as another colobine species such
Figure4Closestdistancebetweenvictimandaggressorafter
Figure 4 Closest distance between victim and aggressor after aggression (n=64) as Trachypithecus francoisi (Wang, 2009). This behavioral
aggression(n=64)
pattern can be explained as a mechanism of reconciliation,
***:P<0.001;**:P<0.01. thussupportingthehypothesisof“increasingsocialtolerance”
topacifytensionwithingroups(Aureli&vanSchaik,1991;de
Dominant individuals showed and did not show relaxed Waal & Ren, 1988), ease anxiety (Cords, 1992; Das et al.,
open-mouthbehaviorwhenapproachingsubordinates47times 1998), reduce continued aggression (Call et al., 1999; Cords,
and 25 times, respectively. Dominant individuals were able 1992;deWaal,1993)anddecreaseheartrates(Smucnyetal.,
to get closer to subordinates when they exhibited this display 1996).
Figure 4 Closest distance between victim and aggressor after aggression (n=64)
behavior(t=7.924,P<0.001)(Figure5). Similar to earlier descriptions (Ren et al., 1990b), relaxed

open-mouthdisplayinR.roxellanaalsohadanaffiliativeeffect,
allowing subordinates to approach dominant individuals more
closely(Figure3). Interestingly,wenotedthatmostindividuals
inthestudygroupalsofrequentlyexhibitedrelaxedopen-mouth
display toward reserve staff during provisioning, suggesting
possibleaffiliationandacceptanceforeasierfoodacquisition.
We also found that relaxed open-mouth display functioned
as reassurance–a kind of affiliative signal displayed by
Figure 5 Distance achieved by a dominant individual approaching a subordinate when shodwoimngi nant individuals towards subordinates to initiate closer
relaxed open-mouth display (n=72) proximity to each other (van Hooff, 1967; Wiper & Semple,
2007) (Figure 5). Dominant individuals can use this behavior
to reassure and ease anxiety in subordinates who may treat
theformerasapotentialthreat(Cords,1992;Dasetal.,1998;
Ren et al., 1990b). This behavior has also been reported
whenadultfemalescarefortheirinfants,whenadultmalesor
Figure 5 Distance achieved by a dominant individual femalessolicit sexualpartnersforcopulation, andwhenadult
Figure 5 Distance achieved by a dominant individual approaching a subordinate when showing
males pacify their own OMUs after conflict between two or
relaxed open-maoputphr odiascphlaiyn g(na=7s2u)b ordinatewhenshowingrelaxedopen-mouth
more adults (Ren et al., 1990b). Thus, reassurance behavior
display(n=72)
maybeinstigatedtoreassureinfants,sexualpartnersandunit
***:P<0.001. memberstogainfitness,socialstabilityandself-assurance.
118 www.zoores.ac.cn
Within OMUs of R. roxellana, the exchange of relaxed stump-tailed macaques: a multivariate approach. Animal Behaviour,
open-mouth display between two individuals yielded more 58(1):165–172.
significant outcomes than when one individual displayed the
Cords M. 1992. Post-conflict reunions and reconciliation in long-tailed
behavior alone, allowing subordinates to approach dominant
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Cui DY, Niu KF, Tan CL, Yang MY, Zhang YY, Zhang JG, Yang YQ.
grooming and hugging (Figure 3), as well as reducing the
2014. Behavior coding and ethogram of Guizhou snub-nosed monkey
distance between victims and aggressors after aggression
(Rhinopithecus brelichi). Sichuan Journal of Zoology, 33(6):815–828. (in
(Bout & Thierry, 2005; van Hooff, 1967) (Figure 4). These
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findings are similar to observations in other non-human
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de Waal, 1986; de Waal & Luttrell, 1989; de Waal & Ren, stress-related behavior of long-tailed macaque aggressors. International
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open-mouth display helps maintain the stability and cohesion
primates.TheQuarterlyReviewofBiology,61(4):459–479.
ofthespecies’multi-levelsocialorganization(Qietal.,2014).
deWaalFBM,RenRM.1988.Comparisonofthereconciliationbehaviorof
We quantitatively analyzed the functions and hypotheses
stumptailandrhesusmacaques.Ethology,78(2):129–142.
of relaxed open-mouth display within OMUs of free-ranging
deWaalFBM,LuttrellLM.1989.Towardacomparativesocioecologyofthe
R. roxellana, which are essential for understanding the social
genusMacaca:differentdominancestylesinrhesusandstumptailmonkeys.
dynamicsandmechanismsofmulti-levelsocieties.
AmericanJournalofPrimatology,19(2):83–109.
COMPETINGINTERESTS deWaalFBM.1993.Reconciliationamongprimates: areviewofempirical
evidenceandunresolvedissues.In: MassonWA,MendozaSP.Primate
Theauthorsdeclarethattheyhavenocompetinginterests. Social Conflict. Albany, NY, USA: State University of New York Press,
111–144.
AUTHORS’CONTRIBUTIONS
GuoS,LiB,WatanabeK.2007.DietandactivitybudgetofRhinopithecus
Y.J.Z. and Z.F.X. designed the study. Z.F.X. supervised the entire study. roxellanaintheQinlingMountains,China.Primates,48(4):268–276.
Y.J.Z. collected and analyzed behavioral data with H.C.C. and Y.X.C.’s Hinde RA, Rowell TE. 1962. Communication by posture and facial
additionalmethodologicalsupports.Y.X.C.andY.J.Z.wrotethemanuscript expression in the rhesus monkey (Macaca mulatta). Proceedings of the
and revised it accordingly. H.C.C., Y.C., H.Y. and W.J.Y. participated in ZoologicalSocietyofLondon,138(1):1–21.
behavioral data collection. H.Y., W.J.Y. and X.D.R. provided necessary LiBG,ChenFG,LuoYS,XieWZ.1993.Majorcategoriesofvocalbehaviour
logisticalsupportsonfieldwork. Allauthorsreadandapprovedthefinal inwildSichuangoldenmonkey(Rhinopithecusroxellana).ActaTheriologica
versionofthemanuscript.
Sinica,13(3):181–187.(inChinese)
Li BG, Li HQ, Zhao DP, Zhang YH, Qi XG. 2006. Study on dominance
ACKNOWLEDGEMENTS
hierarchyoftheSichuansnub-nosedmonkey(Rhinopithecusroxellana)in
We thank the Administration Bureau of Shennongjia National Nature QinlingMountains.ActaTheriologicaSinica,26(1):18–25.(inChinese)
Reserve for their support, and Cheng Guo, Lang Lu and Bo Zhang for LiY,RenBP,LiYH,LiDY,HuJ.2013.BehaviorethogramandPAEcoding
additional assistance on the study and manuscript. We are grateful for systemofRhinopithecusbieti.SichuanJournalofZoology,32(5):641–650.
editor-in-chief, Yong-Gang Yao, and two anonymous reviewers who offer (inChinese)
preciouscommentsandsuggestionsonrevisionofthemanuscript.
Martin P, Bateson P. 1993. Measuring Behavior: An Introductory Guide.
Cambridge:CambridgeUniversityPress,50–55.
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