生物学

SHORTCOMMUNICATION

Therelationshipbetweenfemalerankandreproductiveparametersoftheringtailedlemur:apreliminaryanalysis

YukioTakahataÆNaokiKoyamaÆShinichiroIchinoÆNaomiMiyamotoÆMasayukiNakamichiÆTakayoSoma

Received:8June2007/Accepted:5November2007/Publishedonline:22December2007ÓJapanMonkeyCentreandSpringer2007

AbstractWeuseddatafroma13-yearfieldstudyofwildringtailedlemurstoanalyzetherelationshipbetweenfemalerankandreproductiveparameters.Inmediumandsmallgroupstherewerenosignificantdifferencesinbirthrate,infantmortalityrate,andthenumberofsurvivinginfantsbetweenthefemalerankcategories.Ontheotherhand,inlargesizedgroupslow-rankedfemaleshadasmallernumberofsurvivinginfantsthanmiddle-rankedfemales.Thissuggeststhatinlargesizedgroups,within-groupcompetitionloweredthevaluesofreproductiveparametersoflow-rankedfemales.Ontheotherhand,highandlow-rankedfemalesofsmallsizedgroupstendedtohaveasmallernumberofsurvivinginfantsthanhigh-rankedfemalesofmediumsizedgroupsandmiddle-rankedfemalesoflargesizedgroups.Between-groupcompetitionshouldlowerthevaluesoftheirreproductiveparameters.Insum,theseresultsfittheexpectationfromWrangham’s(1980)intergroupfeedingcompetitionmodel.

Y.Takahata(&)

SchoolofPolicyStudies,KwanseiGakuinUniversity,2-1Gakuen,Sanda669-1337,Japane-mail:z96014@kwansei.ac.jpN.Koyama

KyotoUniversity,Kyoto,JapanS.Ichino

GraduateSchoolofScience,KyotoUniversity,Kyoto,Japan

N.MiyamotoÁT.Soma

GraduateSchoolofAsianandAfricanAreaStudies,KyotoUniversity,Kyoto,JapanM.Nakamichi

FacultyofHumanSciences,OsakaUniversity,Osaka,Japan

KeywordsLemurcattaÁFemalecompetitionÁRankÁReproductiveparametersÁBirthrateÁInfantmortality

Introduction

Thereisnoclearrelationshipbetweenfemalerankandreproductivesuccessinprimates(Fedigan1983).Somestudieshavereportedapositiveassociationbetweentheseparameters(e.g.,NoordwijkandSchaik1999;Cheneyetal.

¨mmerliandMartin2004),whereasothershavenot(Ku

2005).However,therearefewdataonthistopicaboutwildandindividuallyidentifiedpopulationsoflemuridspecies.Theringtailedlemur(Lemurcatta)isadiurnalprosimianspecies,formingamatrilineal/female-bondedgroup(Jollyetal.2002).Itmaybeasuitablespeciesforanalyzinghypothesesconcerningfemalecompetitionsincethefemalesareexposedtoseveredualcompetition(withinandbetween-groupcompetition).Takahataetal.(2006)foundthatthebirthrateandthemeannumberofsurvivinginfantsgeneratedaninvertedU-shapedcurvewhenplottedagainstthenumberofadultfemales,butthattheinfantmortalitydidnothaveaconsistentcorrelationwiththenumberofadultfemalemembers.ThesefindingsweresimilartothepredictionsofWrangham’s(1980)intergroupfeedingcompetition(IGFC)hypothesis.

Ontheotherhand,withinaringtailedlemurgroup,femalestendedtobelinearlyranked,andtheyfrequentlyexhibitedseverecompetitivebehaviorsfordominancerankagainsteachother(Koyamaetal.2005).Inthisreport,basedondatafroma13-yearfieldstudy,weanalyzereproductivedataofwildringtailedlemursinordertoevaluatethecorrelationbetweenfemaledominancerankandreproductiveparameters.

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136Subjectsandmethods

Thisstudywascarriedoutfrom19to2001atBerentyReserve,SouthernMadagascar(fordetailsonthehistoryandhabitatofthisreserve,seeJollyetal.2002).Theringtailedlemurisastrictseasonalbreeder,andbirthsoccurbetweenlateAugustandlateDecemberatBerenty.Basedondemographicdata,wecalculatedbirthrate(BR;theproportionofadultfemaleswhogavebirthineachbirthseason),infantmortalityrate(IMR;theproportionofinfantswhodiedwithin1yearafterbirth),andmeannumberofsurvivinginfants(NSI)1yearafterbirthperadultfemale.Weusedbirthdatafor60group-yearsandinfantmortalitydatafor57group-yearsrecordedforTroopsCX,C1,C2,C2A,C2B,T1,andT2,andtheHSKgroup(Table1)(fordetailsofthesetroops,seeKoyamaetal.2002).Infantmortalitydataforthreegroup-yearswereexcludedbecauseofincompleteinformation.

Femalesaged3yearsormoreandprimiparous2-year-oldfemaleswereconsideredadults.Dominanceranksweredeterminedonthebasisof:1.approach–retreatinteractionswhilefeedinganddrink-ing,and

2.

submissivevocalizations(spat-call).

WhenfemaleAwasdisplacedfromfoodorwaterasaconsequenceoffemaleB’sapproach,orwhenfemaleAspat-calledtofemaleB,femaleAwasconsideredtobesubordinatetofemaleB(Koyamaetal.2005).Therelativeranksofadultfemaleswerecalculatedforeachstudyyearusingaformulathatindexedthealphaanimalas100%andthelowestrankinganimalas0%.Theformulawasasfollows:

Relativerankofanadultfemaleð%Þ¼ðNÀRÞÄðNÀ1ÞÂ100

Table1NumberofobservationyearsforeachstudygroupGroupBirth(years)Infantmortalityandnumberofsurvivinginfants(years)CX88C11212C288C2A54C2B54T44T198T288HSK11Total

60

57

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N:numberofadultfemalesinthegroupR:rankofthefemalewithinthegroup

Takahataetal.(2006)reportedthatgroupsizeinfluencesreproductiveparametersoffemaleringtailedlemursatBerenty.BRandNSIgeneratedaninvertedUshapedcurvewhenplottedagainstgroupsizeandnumberofadultfemalemembers,butIMRdidnothaveaconsistentcor-relationwithgroupsizeandnumberofadultfemalemembers.Therefore,wedividedtheentiredatasetintothreegroupsofdifferentsizes,basedonthenumberofadultfemales:large(eight–ninematurefemales),medium(four–sevenmaturefemales),andsmall(two–threematurefemales).Ineachsizedgroup,femalesweregroupedintothreerankcategories:highrank(100–66.8%),middlerank(66.7–33.4%),andlowrank(33.3–0%).Thus,femalesweredividedintoninegroups,basedongroupsizeandrankcategory.StatisticalanalyseswereperformedusingExcel2002(Microsoft2001)andStatistica(StatSoft1999).ThelevelofsignificancewasP\\0.05.Alltestsweretwo-tailed.

Results

Withineachsizedgroup

Insmallsizedgroups,therewasnosignificantdifferencebetweenfemalerankcategoriesofhigh,middle,andlowinBR(one-wayANOVA,F(2,45)=0.916,P[0.4),IMR(F(2,22)=0.842,P[0.4),andNSI(F(2,39)=1.026,P[0.3).Inmediumsizedgroups,therewasalsonosig-nificantdifferencebetweenfemalerankcategoriesinBR(F(2,175)=0.438,P[0.6),IMR(F(2,139)=2.278,P[0.1),andNSI(F(2,169)=1.54,P[0.2).Inlargesizedgroups,therewasnosignificantdifferenceinBR(F(2,96)=0.694,P[0.5)andIMR(F(2,)=1.316,P[0.2)betweenfemalerankcategories.Ontheotherhand,therewasasignificantdifferenceinNSI(F(2,90)=3.728,P\\0.03).Apost-hoctestshowedthatlow-rankedfemalesexhibitedlowervaluesofNSIthanmiddle-rankedfemales(Duncan’smultiplerangetest,P\\0.01).Incon-trast,therewerenosignificantdifferencesinNSIbetweenhighandmiddle-rankedfemales(P[0.1),andbetweenhighandlow-rankedfemales(P[0.1).

Betweengroupsofdifferentsizes

Inthepooleddataofallstudygroups,therewasasignificantdifferenceinBR(one-wayANOVA,F(8,316)=2.300,P\\0.03)andNSI(F(8,298)=2.751,P\\0.01)(Fig.1).Incontrast,therewasnosignificantdifferenceinIMR

Primates(2008)49:135–138(F(8,225)=1.504,P[0.1)(Fig.2).Posthoctestspro-ducedthefollowingresults:1.

High-rankedfemalesofsmallgroupsexhibitedlowerBRvaluesthanmiddle-rankedfemalesofmediumsizedgroups(Duncan’smultiplerangetest,P\\0.05)(Fig.1).Similarly,low-rankedfemalesofsmallsizedgroupsexhibitedlowerBRvaluesthanmid-rankedfemalesoflargesizedgroups(P\\0.02).TheyalsoexhibitedlowerBRvalesthanhigh-rankedfemales(P\\0.02),mid-rankedfemales(P\\0.01),andlow-rankedfemales(P\\0.02)ofmediumsizedgroups.TherewasnosignificantdifferenceinBRinothercombinationsoffemalegroups.

2.TherewerenosignificantdifferencesinIMRinanycombinationoffemalegroups(Fig.2).

3.

High-rankedfemalesofsmallsizedgroupsexhibitedalowervalueofNSIthanhigh-rankedfemalesofmediumsizedgroups(Duncan’smultiplerangedtest,P\\0.02)andmiddle-rankedfemalesoflargesizedgroups(P\\0.05)(Fig.3).Similarly,low-rankedfemalesofsmallsizedgroupsexhibitedalowervalueofNSIthanhigh-rankedfemalesofmediumsizedgroups(P\\0.02),andmid-rankedfemalesoflargesizedgroups(P\\0.05).Low-rankedfemalesoflargesizedgroupsshowedalowervalueofNSIthanhigh-rankedfemalesofmediumsizedgroups(P\\0.02).Besides,low-rankedfemalesexhibitedlowervaluesofNSIthanmiddle-rankedfemalesinlargesizedgroups(P\\0.05).TherewasnosignificantdifferenceinBRinothercombinationsoffemalegroups.

SEFig.1FemalerankcategoriesandBRineachsizedgroup.Large-highhigh-rankedfemalesoflargesizedgroup;Large-midmid-rankedfemalesoflargesizedgroup;Large-lowlow-rankedfemalesoflargesizedgroup;Medium-highhigh-rankedfemalesofmediumsizedgroup;Medium-midmiddle-rankedfemalesofmediumsizedgroup;Medium-lowlow-rankedfemalesofmediumsizedgroup;Small-highhigh-rankedfemalesofsmallsizedgroup;Small-midmiddle-rankedfemalesofsmall-sizedgroup;Small-lowlow-rankedfemalesofsmall-sizedgroup.*P\\0.05;**P\\0.01137

Fig.2FemalerankcategoriesandIMRineachsizedgroup.Forfemalerankcategories,seethelegendofFig.1Discussion

Weanalyzedreproductivedataofwildringtailedlemursinordertoinvestigatetherelationshipbetweenfemaledominancerankandreproductiveparameters.Severaltendenciesareapparentfromthisstudy.1.

High-rankedfemalesdidnotalwaysattainhighvaluesofbirthrateandnumberofsurvivinginfantsinallsizedgroups,contrarytowhathasbeenfoundforlong-tailedmacaques(vanNoordwijkandvanSchaik1999)andchacmababoons(Cheneyetal.2004).Thisresultiscontrarytoexpectationsbecausefemaleringtailedlemursfrequentlyfightforhigherrank.AtBerenty,Pride(2005)analyzedfecalcortisolconcentrationstoassessstressofringtailedlemurs.Hefoundthatcortisollevelsdidnotdifferbetweendominantandsubordinatefemales,andpointedoutthatthediffer-enceinstressbetweendominantandsubordinatefemalesremainsspeculative.Furtherbehavioralandphysiologicalresearchisneededtoclarifythesepoints.

Fig.3FemalerankcategoriesandNSIineachsizedgroup.Forfemalerankcategories,seethelegendofFig.1.*P\\0.05123

1382.

Inmediumandsmallsizedgroups,therewerenosignificantdifferencesbetweenfemalerankcategoriesinreproductiveparameters,asreportedforMacaca

fuscata(Wolfe1984)andM.sylvanus(Ku

¨mmerliandMartin2005).Incontrast,inlargesizedgroups,low-rankedfemalesexhibitedalowervalueofNSIthanmiddle-rankedfemales,whichsuggeststhattheyfacedseverewithin-groupcompetition.Thus,within-groupcompetitionmaybemoreintenseinlargegroups,justasvanNoordwijkandvanSchaik(1999)foundforwildlong-tailedmacaques.Pride(2005)foundthatmeancortisollevelswerehighinverylargegroups.Insuchasituation,socialstressmighthaveloweredthereproductiveparametersoflowerrankedfemales.AtBerenty,groupevictions/fissionsfrequentlyoccurwhengroupsarelarge(mean22.5,range16–28)andincludedatleastsevenadultfemales(mean8.4,range7–10)(IchinoandKoyama2006).Thesedatasuggestthat,inlargesizedgroups,femalesshouldreducetroopsizebyevictingotherfemalesfromgroupsthrough‘‘targetedaggression’’,justasdescribedbyVickandPereira(19)andPereira(1995),inordertopreventadeclineinreproductivesuccess.

3.

Insmallsizedgroups,thehigh-andlow-rankedfemalesexhibitedlowervaluesofBRandNSIthanthoseofmediumsizedgroups.Pride(2005)alsopointedoutthatfemalesinthesmallestgroups(mean5.5animals)hadsignificantlyhighercortisollevelsthanallothergroups.Thereisapossibilitythatfemalesinsmallsizedgroupssufferfromincreasedbetween-groupcompetitionduetothehighpopulationdensityinourstudyarea(542.3individuals/km2in2001),andthatsuchsocialstresshasloweredtheirreproductiveparameters.Furtheraccumulationofdatawillclarifytherelationshipbetweendemographicandsocialfactors(e.g.,population/groupdensity,groupsize,rank,etc.)andthefemalereproductivesuccessoffemale-bonded/matrilinealprimates.

AcknowledgmentsWethankM.DeHeaulmeandhisfamilyfortheirkindpermissiontocarryoutthisstudyatBerentyReserve;A.Randrianjafy,directoroftheBotanicalandZoologicalParkofTsimbazaza,andtheGovernmentoftheMalagasyRepublic,fortheir

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kindpermissiontoperformthisresearchinMadagascar;andY.Kawamoto,H.Hirai,andA.Jollyforcooperationinfieldwork.ThisworkwassupportedbyaGrant-in-AidforScientificResearchtoN.Koyama(No.06610072andNo.05041088)andtoY.Takahata(No.120700).

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