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PLOSONE:DomesticCats(Felissilvestriscatus)DoNotShowSignsofSecureAttachmenttoTheirOwners

Domestic Cats (Felis silvestris catus) Do Not Show Signs of Secure

Attachment to Their Owners
AlicePotter, DanielSimonMills
Published:September2,2015

DOI:10.1371/journal.pone.0135109

Abstract

TheAinsworthStrangeSituationTest(SST)hasbeenwidelyusedtodemonstratethatthebondbetweenbothchildrenanddogsto
theirprimarycarertypicallymeetstherequirementsofasecureattachment(i.e.thecarerbeingperceivedasafocusofsafetyand
securityinotherwisethreateningenvironments),andhasbeenadaptedforcatswithasimilarclaimmade.Howevermethodological
problemsinthislatterresearchmaketheclaimthatthecatownerbondistypicallyasecureattachment,operationallydefinableby
itsbehaviourintheSST,questionable.WethereforedevelopedanadaptedversionoftheSSTwiththenecessarymethodological
controlswhichincludeafullcounterbalanceoftheprocedure.Acrossoverdesignexperimentwith20catownerpairs(10each
undertakingoneofthetwoversionsoftheSSTfirst)andcontinuousfocalsamplingwasusedtorecordthedurationofarangeof
behaviouralstatesexpressedbythecatsthatmightbeusefulforassessingsecureattachment.Sincedatawerenotnormally
distributed,nonparametricanalyseswereusedonthosebehavioursshowntobereliableacrossthetwoversionsofthetest(which
excludedmuchcatbehaviour).Althoughcatsvocalisedmorewhentheownerratherthestrangerleftthecatwiththeother
individual,therewasnootherevidenceconsistentwiththeinterpretationofthebondbetweenacatanditsownermeetingthe
requirementsofasecureattachment.Theseresultsareconsistentwiththeviewthatadultcatsaretypicallyquiteautonomous,
evenintheirsocialrelationships,andnotnecessarilydependentonotherstoprovideasenseofsecurityandsafety.Itisconcluded
thatalternativemethodsneedtobedevelopedtocharacterisethenormalpsychologicalfeaturesofthecatownerbond.
Citation:PotterA,MillsDS(2015)DomesticCats(Felissilvestriscatus)DoNotShowSignsofSecureAttachmenttoTheir
Owners.PLoSONE10(9):e0135109.doi:10.1371/journal.pone.0135109
Editor:AtsushiSenju,Birkbeck,UniversityofLondon,UNITEDKINGDOM
Received:June5,2013Accepted:July18,2015Published:September2,2015
Copyright:2015Potter,Mills.ThisisanopenaccessarticledistributedunderthetermsoftheCreativeCommons
AttributionLicense,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthor
andsourcearecredited
Funding:Thisworkwasnotexternallyfunded,butwasundertakeninpartialfulfillmentoftheMScofAlicePotter.Nocurrent
externalfundingsourcesforthisstudy.
Competinginterests:Theauthorshavedeclaredthatnocompetinginterestsexist.
Introduction

Thedomesticcat(Felissilvestriscatus)hasrecentlypassedthedogasthemostpopularcompanionanimalwithinEurope[1],[2].
Easeofcare,abilitytoliveinasmallresidenceandthecapacitytocopewithbeingleftaloneforlongperiodsoftimehavebeen
reportedasreasonsforthispopularity[1],[3],[4],[5].Indeed,somehavesuggestedthatcatsareidealcompanionsforowners
whoworklonghours[5].However,thereisevidencetoindicatethatsomecatsmayshowsignsofseparationdistressinthe
absenceoftheirowner[6]andithasbeensuggestedthatthecatownerbondmaybeaformofattachmentsimilartothatwhich
existsbetweenadogorchildanditsprimarycarer[7].Bowlby[8][9]describedattachmentasanenduringpsychologicalbond,that
servestoimproveaninfantschancesofsurvivalbykeepingitclosetoitsmother.Inthiscontextthetermattachmenthasa
preciseoperationaldefinitionrelatingtotheprovisionofsafetyandsecurity,andisnotsimplyanaffectionatebondithasseveral
objectivelydefinablecharacteristics:attachedindividualsseektomaintainproximityandcontactwiththeattachmentfigure,
attachedindividualsbecomedistressedwheninvoluntarilyseparatedandshowsignsofpleasureupontheirreturn,attachment
figuresactasasafehaventowhichtheattachedindividualwillreturnwhenfrightenedbytheenvironment,attachmentfiguresact
asasecurebasefromwhichtheattachedindividualcanmoveoffandengageconfidentlyinactivities[10].Noneofthesealoneis
sufficienttodemonstrateorinfersecureattachment,butmanyofthesefeaturesareassessedwithintheStrangeSituationTest
(SST)developedbyAinsworth[11]forthispurpose.Theprocedureinvolvesplacingasubjectinanunfamiliarroom(strange
situationtoprovokeasenseofinsecurity)togetherwithitscarer(potentialattachmentfigure)andastranger(socialcontrolto
whichthereshouldbenoattachment)followedbyaseriesofepisodesofseparationfrom,andreunionswith,theircarerandthe
stranger.Thenormalhealthyresponseinthiscontextinvolvesadifferentiationbetweenthecarerandthestrangerinthesupport
theyprovidetothesubjectinthischallengingenvironment.Thiscanbeusedtoimplythetypeofattachmentthatexistsbetween
thesubjectandcare.Inthiswayasecureattachmentstylecanbeoperationallydefinedotherstylesofresponseareconsidered
problematic[11].Thetestwasoriginallydevelopedtoinvestigatemotherinfantattachment,buthasbeenusedandadaptedfor
studyingattachmentbetweenotherspeciesandtheircarerse.g.chimpanzees[12],dogs[13],[14],[15],[16],[17],[18],[19],[20]
andhandrearedwolves[17].Itsapplicationtodogswasinspiredbytheresemblanceofthedogownerbondtothatwhichexists

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betweenachildandparent[13],[14]andthereisnowstrongevidencetoindicatethatthetypicaldoghumanbondalsoincludes
therequirementsofasecureattachmentdefinedinthisway[18].Thewelldevelopedsocialityofdogsmaybeparticularlyimportant
inthisregard[14].Nonethelessbothcatsanddogsappeartoshowseparationrelatedproblems,whichithasbeensuggested
mightbeassociatedwithattachmenttoowners[21]anditisincreasinglyrecognisedthatcats(Felissylvestriscatus)areperhaps
moresocialthantraditionallythoughtevenwiththeirownspecies[22],[23],[24],[25],[26],[27],[28],[29].Cooperativecoloniesof
relatedfemalesarisingasaresultoftheavailabilityofkeyresourcesarewelldocumented[24],[25],butevenmalecats,especially
thoseneutered,areknowntobesocial[28].Preferredassociatesmaybeidentifiedfromaffiliativebehaviourssuchasallorubbing
andallogrooming[22]andthistypeofactivitymaybeusedtoassessthesocialbondthatexistsbetweentheindividualsinvolved
[26].Itisthereforeclearthatcatshavethecapacitytoformsocialintraspecificrelationships,andthismayunderpintheformof
relationshiptheyformwithhumans,especiallythosewithwhomtheyshareahome.
Theextenttowhichcatsdemonstratesocialitytowardshumansappearstobeinfluencedbyawiderangeoffactors[30],[31].
Kittensarereportedtohaveasensitivephaseofsocialisationtowardshumansbetweentheirsecondandseventhweekoflife[32].
Duringthistimeexposuretohumans,amountofhandling,numberofhandlersandpresenceofthequeenhaveallbeenfoundto
influencesocialitytowardshumans[32],[33].Arangeofhumanrelatedfactorsalsoinfluencethedevelopmentofthesocial
behaviourexpressedbycatstowardspeople[34],[35].Giventhesefindingsandthetendencyofownerstoconsiderpetcatsas
partofthefamily[36],itseemsreasonabletoexaminewhetherthetypicalbondshownbypetcatstowardstheirownersalso
involvesaformofsecureattachmentthatprovidesadditionalsafetyandsecurity.UsingamodifiedversionoftheAinsworthSST,
Edwardsetal.,[7]haveclaimed,onthebasisofapreliminarystudy,thatthisisindeedthecase.Theyreportedthatcatsonly
playedinthepresenceoftheirowner,vocalisedmorewhenleftalone,engagedinmorelocomotion/explorationwhiletheowner
waspresentandweremorealertinthepresenceofthestranger[7].HowevertheirconclusionthattheiruseofamodifiedSST
demonstratesthatthecatownerbondtypicallymeetstherequirementsofasecureattachmentisquestionableonseveralgrounds,
duetomethodologicalflawsintheirstudy,whichmightaccountforthedifferencesobserved.Firstly,theexperienceofthecatwithin
theprocedureinrelationtotheownerandstrangerwasnotequivalent.Forexamplewhenanalysingthecatsbehaviourtowards
theowners,Edwardsetal.,[7]usedatafromtwoepisodeswithinthetest,neitherofwhichfollowanepisodeofthecatbeingalone,
whereastheassessmentofthecatsbehaviourtowardsthestrangersdependsononlyoneepisodewhichfollowsanepisodeof
isolation.Thedifferentconditionsappliedtothecatsinthetimeprecedingtheepisodewhenitisalonewiththeownerandstranger,
maythereforeexplaindifferencesinthecatsbehaviourtowardstheseindividualsratherthantherelationshipthecathaswitheach
ofthem.Secondly,Edwardsetal.,[7]alsofailtocontrolforapossibleepisodeordereffect.Episodeorderdescribesthesequence
inwhichtheownerandstrangerparticipateintheprocedureandthishasthepotentialtoaffectthecatsbehaviour,asthecatmay
alteritsbehaviourinrelationtothestrangesituationovertime,regardlessofwhoispresent.Theuseofacounterbalanced
procedureinwhichthesequenceisreversedforhalfofthesubjectscancontrolforthispotentialconfound[18].Thirdly,Edwardset
al.,[7]didnotanalysethedatafromallepisodes,butonlyfourofthem(episodes47).Thismeanttheirdatacamefrom6minutes
ofobservationofthecatwiththeowner,3minuteswiththestrangerand3minuteswhenthecatwasalone.Thisagainconfounds
theabilitytoascribedifferencesinbehaviourtowardsthetwotypesofhumansubjectinvolvedinthetesttotherelationship,rather
thantothemethodologicalfeaturesofthestudy.Finally,itisalsoassumedbyEdwardsetal.,[7]thatthecatbehaviourobservedis
reliable,(i.e.thatagivencatwouldconsistentlyshowthistypeofresponseinthistypeofsituation)giventhelargenumberof
variablesassessed,spuriousfindingsduetoTypeIstatisticalerrorsarearisk.Thereforethestudyreportedherereexaminedthe
issueofsecureattachmentbycatstotheircarers,inawaythataddressestheseconcernsbyusingacrossoverdesignexperiment
withanimprovedandcounterbalancedmodificationoftheAinsworthSST.Ourfirstaimwastoassesstherobustnessofpotential
measuresofcatattachmentwithintheSSToursecondaimwastoassesswhetherthosebehavioursfoundtobesuitablyrobust
andrelevantindicatethatthecatownerrelationshipmeetstherequirementsofasecureattachmentasdefinedwithintheSST.
MaterialsandMethods

Ethicsstatement

Aspartoftheprotocolforthisstudy,allownersprovidedwritteninformedconsenttotheirandtheircatsparticipation.Ownerswere
allowedtowithdrawthisconsentatanytimewithoutgivingreason,andnodatafromthesesubjectswouldbeused.Thefull
protocol,includingconsentprocedures,wasapprovedbytheUniversityofLincolnSchoolofLifeSciencesResearchEthics
Committee,afterspecificconsiderationoftheethicalfactorsrelatingtoboththehumans(ownersEA2)andnonhumananimals
(catsEA3)involved.
SubjectsandParticipants

Aconveniencesampleoftwentyownercatdyadswasrecruitedthroughpersonalcontactandadvertisementsinlocalpetrelated
businesses.Allparticipantslivedwithin5miles(8km)ofthetestarea.Ownerswerealladults,withfourmalesand16females
agreeingtotakepart.Abroadspectrumofownershiplifestyleswererepresented,withtenoftheownersinfulltimeemployment,3
inparttimeemployment,3studentsand2unemployed.Thecatsubjectswere13malesand7femaleswhoseagesranged
between19yearsold(meanageSD5.05years3.17).Onefemalecatandallmaleshadbeenneutered,andnoentirefemale
wasinseason.TwocatswerepedigreeBritishShorthairsandtheremaining18subjectswereDomesticshorthairs(15)and
Domesticlonghairs(3).Allcatshadbeenintheircurrenthomeforaminimumoftenmonths.Elevenofthecatslivedwithatleast
oneothercat(range14)andtwolivedwithadoginthehome.Nineteenofthecatshadregularaccesstotheoutside.Allcats
werefreefromeitherovertorknownongoingmedicalconditions.Allbutoneownerprovidedinformationrelatingtotheexperience
ofthecatsofstrangesituations.Onlytwohadmuchexperienceofstrangesituationsawayfromthecurrentowner,sincebeing
takeninbythecurrentowner(havinglivedawayfromtheownerforaperiodoftime),eightwereknowntohavemovedhomewith
theowner.Allexceptoneofthecatswereusedtobeingtransportedinacatcarrier.
Testingareaandmaterials

Twosimilar,plainroomswereusedforthestudy(Fig1),inordertoensureanequivalentstrangephysicalenvironmentineachtest.
Testroomswereunfamiliartoallcatsubjects.Bothroomswereequippedwithtwochairs(fortheownerandstranger),threecat
toys(twoballsandastringandrodtoy)andasmallarea(approx.80cmby75cmby35cm,withapartiallyoccludedentrance)in
whichcatscouldhide.Windowsinbothroomswerecoveredtoavoidanyvisualdistractionfromoutside.Withinbothroomsavideo
camera(FlipVideoUltraHD)mountedonatripodwassetuptorecordthetestperiodandawebcameraconnectedthroughalive
feedtoamonitorlocatedoutsidethetestroomwasmountedaboveeachdoorway.Thewebcameraallowedboththeexperimenter
tofollowtheprocedureandtheownerstoobservetheircatduringepisodesinwhichtheywerenotpresent.Theroomswere

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dividedbystripsofwhitetapeintofourzones:i)regionaroundownerschair,ii)regionaroundstrangerschair,iii)door,iv)play
area(Fig1).Inordertocontrolforanyeffectsofspatiallocationofowner,theownerswerepseudorandomlyassignedtooneofthe
twochairsavailable(Fig1)inthefirsttestandthenallocatedtheotherchairintherepeattest.Thetestroomsandallequipment
werethoroughlycleanedwithanenzymaticcleaner(UrineOffforCatsandKittens)beforeandaftereachtesttoremovecatrelated
odours,betweentests.

Fig1.Graphicalillustrationoflayoutanddimensionsoftestingrooms(1)and(2),EachroomwasdividedintofourareasA)owner/stranger,B)
owner/stranger,C)door,D)play.

doi:10.1371/journal.pone.0135109.g001
Procedure

Theprocedurecomprisedoftwoconditions:modified(A)andreversedmodified(B)versionoftheAinsworthSSTbothconsistingof
nine3minuteepisodesinwhichthecatiseitheraloneorwiththeownerand/orastrangerinordertoassesshowitrespondstoa
seriesofproceduresdesignedtoalterthelevelandformofsocialsupportavailabletoit,ortriggerseekingoutofanattachment
figure(seeTable1fordetailsoftheproceduresandDatacollectionandanalysisplanbelowfordetailsofthespecificpredictions
madeindifferentcircumstancesifacatissecurelyattachedtoitsowner).Hereaftertheconventionofaletterfollowedbyanumber
isusedtorefertoconditionsandepisodesasdescribedinTable1.Hence,A2referstoconditionAepisode2.TheAinsworthSST
wasextendedfromsixtonineepisodesinordertoallowtheownerandstrangertotakepartinanequalnumberofepisodes,
separationsandreunionswiththecatsubjects.AswiththeoriginalAinsworthprocedurethedurationofeachepisodewasthree
minutes.InconditionBtheepisodeorderofconditionAwasreversed.Thisreversalofepisodesequencebalancedtheorderin
whichtheownerandstrangerparticipatedintheprocedureacrossthetwotests(Table1).

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Table1.Outlineofepisodesequenceandprotocolforthemodified(A)andreversed(B)StrangeSituationTestconditions.

Thefollowingeffectsacrosstheepisodeswouldbeconsistentwithsecureattachmenttowardsthecareroverthesocial
control(stranger)increasedpassivebehaviour,explorationandsocialplayinthepresenceofthecarergreaterseekingof
proximityandattemptstomaintainproximity/contactwiththecarergreatervocalisationwhenseparatedfromthecarer
increasedvigilanceandorientationtothedoorwhenthecarerisabsent.
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Allownercatpairsparticipatedinbothconditions(AandB)indifferentroomssetupfortheprocedure,andweretestedwithin5
minutesofarrivalatthetestsite.Tensubjectswerepseudorandomlyassignedtogroup1(conditionAfollowedbyconditionB)and
theothertentogroup2(conditionBfollowedbyconditionA).Forallsubjectsaperiodofatleasttwoweekselapsedbetween
participationinthetwoconditions.Twofemalesofsimilarheight,buildandappearancewereusedasthestranger(oneforeach
condition).TestingwasconductedoverasevenweekperiodbetweenMayandJuly2012.Toaccommodatetheschedulesof
subjectsthetestswereconductedatavarietyoftimesbetween09:30and19:00MondaytoSunday.Onaveragetestsonthesame
subjectwereconductedwithinanhourofthesametimeofdayonthetwooccasions(meandifference51.75mins,mode=0).
Datacollectionandanalysisplan

Followingapilotstudyandreviewofpreviousresearch[7],alistofbehaviourswasdrawnupforrecording(SeeS1File).
ContinuousfocalsamplingofvideorecordingsofthecatsbehaviourwasundertakenusingSolomonCoder(Beta12.07.10)to
recordthedurationofthesebehaviours[37]duringeachepisodeofeachcondition.Inordertominimisethesubsequentriskof
errorduetomultiplestatisticaltesting,somefunctionallyrelatedbehaviouralcategoriesweregrouped.Specificallypassive
exploration,activeexplorationandlocomotionweregroupedintoexploration/locomotionandapproaching/orientationtoa
personandfollowingweregroupedintoproximateowner/stranger.Behaviouralmeasureswerethenclassifiedaprioriaccording
totheirputativerelationshiptooneormoreoftheoperationallydefinablecharacteristicsofattachment,andonlythesemeasures
consideredforstatisticalanalysis(Table2).Threecharacteristicsofattachment(proximity/contactseeking,securebaseeffectand
distressduetoseparation)couldbeassessed.Firstly,theownershouldbeapreferredsocialcompaniontothestrangeras
evidencedbythecatseekingproximityandattemptingtomaintainproximity/contactmorewiththeownerthanwiththestranger.
Secondly,iftheowneractsasasecurebase,itwaspredictedthatthereshouldbemorepassivebehaviour,explorationandsocial
playinthepresenceoftheownercomparedtothepresenceofthestranger.Thirdly,catsshouldbemoredistressedbythe
absenceoftheownerthanthestranger,andsoitwaspredictedthatcatsshouldvocalisemorewhenseparatedfromtheowner
comparedtothestranger,andshowgreatervigilanceandorientationtothedoorwhentheownerisabsentcomparedtothewhen
thestrangerisabsent.Nosinglemeasurewouldbesufficienttoconcludethattherelationshipbetweenthecatanditsownerisa
secureattachment,rathertheevidencefromallofthesetestswouldneedtobeconsideredoverall.

Table2.Listofbehavioursstatisticallyanalysedandthecorrespondingcharacteristicofattachmenttheymayindicate.

SeeS1Filefordefinitionofthespecificbehavioursasusedfortheiridentificationfromthevideo.
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Anycatsubjectswhoremainedinthehidingplacethroughouttheexperimentaltestingprocedureswereremovedfromthedata
analysis,sincetheyprovidednousefuldata.
AllstatisticalanalysiswasconductedinMinitab16(MinitabLtd).NormalitywasassessedusingaKolmogorovSmirnovtestand
sincedatawerenotnormallydistributedanonparametricanalysiswasundertaken,inaccordancewiththeproceduredescribedby
JonesandKenward(2003)[38]fortheanalysisofcrossoverdesignexperiments.
Assessmentofthereliabilityofthebehaviourofcatsincomparablesituations.

Inthefirstinstanceitwasimportanttoestablishthereliabilityofthebehaviourthathadthepotentialtobeusedtoassess
attachmentbycats.Thecounterbalancingoftheprocedureandwithinsubjectsdesignoftheexperiment,meantthatitwaspossible
tosystematicallyanalysethedatatodetectsignificantdifferencesinthebehaviourwithinsubjectsinthesamecircumstancesbutat
differenttimes.Thisallowedarigorousassessmentoftherobustnessofeachpotentialmeasure,usingthefollowingprocess.
Comparablemeasuresofbehaviourbasedoneithersingleepisodes(e.g.vocalisingduringA2versusB6)orcombinationsof
episode(e.g.vocalisinginthetwoepisodesA2andA8versusB6andB4)wereidentified(seeS2Fileforafulllist).Next,in
accordancewithJonesandKenward(2003)[38],theoccurrenceofasignificantinteractionbetweentheorderinwhichsubjects
weretested(testorder)andtheconditiononagivenbehaviourwasexaminedfirstusingaMannWhitneytest.Onlyiftherewasno
significantinteractioncouldthebehaviourbetakenforwardforfurtherconsiderationasapotentiallyusefulmeasure.Thenextstage
ofanalysisexaminediftherewasasignificanttestordereffectonthegivenbehaviour.Ifasignificanttestordereffectwasfound
thenthatbehaviourcouldnotbeusedinanyanalysisofattachmentbetweenthetwoconditions(AversusB).Next,becauseeach
socialsituationwasreplicatedwithinacondition,thesignificanceofanyepisodeordereffectonthebehaviourwasexamined(i.e.
theeffectoftimewithinatest).Ifasignificantepisodeordereffectwasfoundthenthatbehaviourcouldnotbeusedinanyanalysis
ofthebehaviourwithinepisodesoccurringatadifferenttimebutwithinthesamecondition.Ifthebehaviourwasaffectedbyboth
testordereffectandepisodeorderthenitcouldnotbeusedasapotentialmeasuretoassessattachment.Onlybehaviour
measuresthatdidnotmeetanyoftheseexclusioncriteriawererobustenoughtoassesswhetherthecatsshowedsignsof
attachmentinthemodifiedSST.

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Individualswhohidduringanentireconditionwereexcludedfromanalyticalconsideration.
AssessmentofattachmentwithinthemodifiedSST.

Followingassessmentofthereliabilityofthepotentialbehaviourmeasures,thosebehavioursthatweredeemedsuitablyrobust
wereusedtodetermineifsignificantdifferencesoccurredwithinsubjectsthatwereconsistentwithsignsofsecureattachmentof
thecattoitsowner,usingWilcoxonssignedranktests.Specifically,thepredictionsoutlinedintheDatacollectionandanalysis
plan(above)weretestedwherethereweresuitabledata.
Results

Twocatsubjects(1maleneutered,6yearsold,1femaleneutered2yearsold)hidduringanentireexperimentaltestingperiodand
werethereforeremovedfromthedataanalysis.Nonewereremovedduetoconcernsovertheirwelfareduringthetest.Thisleft
datafrom18subjectsforanalysis.Themediandurationandinterquartilerangeofthebehavioursofinterestinthetwoconditions
areshowninFig2.Thisappearstoshowwidespreadinconsistencyinthecatsbehaviouracrossthetwoconditions.Thishighlights
theneedtoassessthescientificreliabilityofthesebehaviours,sincebehavioursthatareinconsistentcannotbeusedtoreliably
assesssupposedlystabletraitssuchasattachment.

Fig2.Mediantime(andinterquartilerange)inseconds,spentinvariousactivitiesbycatsinthetwoconditions.

DarkerbarreferstoconditionAandlighterbartoconditionB.
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FullresultsfromtheassessmentofbehaviouralreliabilitycanbefoundintheS3File,butinthefollowingsectionsweconsider
furtherthevalueofthevariousbehavioursthatcouldpotentiallycontributetotheassessmentofdifferentfacetsofattachment,
startingwiththeirrobustnessaspotentialpsychometricmeasures.Tobesuitable,measuresofthesamesituationshouldshowno
significantinteractionbetweentheorderinwhichsubjectsweretested(testorder)andthecondition.Theoccurrenceofa
significanttestordereffectforthesamesituationwithinaconditiondoesnotprecludetheuseofthatmeasurewithinacondition,
butitdoesprecludeitsuseformakingcomparisonsbetweentheconditionsduetotheordereffect.Likewise,anyevidenceofa
significantepisodeordereffectforthesamesituationwithinaconditionprecludestheuseofthatmeasurefromanyanalysisof
episodesoccurringatdifferenttimeswithinacondition,butdoesnotprecludeitsusebetweencomparablesituationsoccurringat
thesametimeinthetwoconditions.However,ifbothatestordereffectandanepisodeordereffectarepresentforthesame
measurewhenusedinsimilarsituationsthenthatmeasurecannotbeusedtomakeanyreliableinferencesfromthetest.
Proximity/contactseeking

Someofthedatarelatingtoproximateowner/strangerwerefoundtoexhibitaninteractioneffect(A2vsB6(S)z=108.5,p<0.05),
andotherdatahadeitheratestordereffect(B5vsA1(O)z=405.5,p<0.05)orepisodeordereffect(B5vsA1(S)z=419.0,
p<0.01)andsothisparameterwasnotusedtoassessattachment.
Someofthedatarelatingtophysicalcontactowner/strangerexhibitedatestordereffect(B4vsA8,z=108.5,p<0.05)andsome
anepisodeordereffect(A1vsB5,z=266.0,p<0.05)andsothisparameterwasnotconsideredsuitableforuseinassessing
attachment.
Markingbehaviourexhibitedanepisodeordereffect(A2+A8vsB6+B4,z=1107.5,p<0.05A1vsB5[markingowner],z=263.5,
p<0.05A1vsB5[markingstranger],z=251.0,p<0.01),butnotestordereffectandsothesedatawereusedincomparisons
relatingtothesameepisodesinthetwoconditionswhererelevanttotheassessmentofattachment.Therewasnosignificant
differenceintheamountcatsmarkedtheownerversusthestrangerinthefirstepisodeoftestA,buttheymarkedtheownermore
thanthestrangerinthefirstepisodeoftestB.Catswerefoundtomarkthestrangersignificantlymorethantheownerwhen
comparingthefirstseparation(A2vsB2)andfirstreunionafterthecatwasalone(A4vsB4),withnosignificantdifference,when
bothwerepresentinepisode5andfollowingthesecondseparationinthenextepisode(A6vsB6),butsignificantlymoremarking
wasdirectedtowardstheownerthanthestrangeratthesecondreunionafterthecathadbeenalone(A8vsB8)(SeeTable3for
statisticalresults).

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Table3.SummaryofattachmentbehaviourresultsfromWilcoxonsignedrankstest.

Key:O=ownerpresent,S=strangerpresent,A1A8=modifiedconditionAepisodes18,B1B8=reversedconditionB
episodes18,Z=Wilcoxonsignedranksteststatistic
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Securebaseeffect

Nointeraction,testorderorepisodeordereffectswerefoundforthemeasuresexploration/locomotionandsocialplay(withthe
ownerorstranger)andthereforetheseparameterswereusedfurthertoassessattachment.Nosignificantdifferenceswerefound
inthedurationoftimecatsspentexpressingexploration/locomotioninthepresenceoftheownercomparedtothestranger(Table
3).Likewisetherewerenosignificantdifferencesinthedurationoftimecatsspentplayingwiththeirownercomparedtoplaying
withthestranger.Inadditiontherewasnosignificantdifferenceintheamountcatsplayedwiththestrangerwhentheownerwas
present(A1)andwhentheownerwasabsent(A2orA8)(Table3).Passivebehavioursexhibitedepisodeordereffects(A2vsB6,
z=368.5,p<0.05A2+A8vsB6+B4,z=023.5,p<0.01)butnotestordereffects.Thereforethisparameterwasusedtoassess
attachmentonlyincomparisonsofthesameepisodenumberbetweenconditions.Catsspentsignificantlymoretimeexpressing
passivebehavioursinthesolepresenceofthestrangerthantheownerinonecombinationofepisodes(A4+A6vsB4+B6,Z=
68.5,N=18,p0.001),butnottheother(A2+A8vsB2+B8).Thissignificantdifferenceinpassivebehavioursisevidentinbothof
theindividualepisodecomparisonsmakingupthiscombinationi.e.betweenA4andB4afterthecathasbeenleftaloneforthefirst
time(Z=2.0,N=18,p0.001)andbetweenA6andB6thefirstdepartureinthesecondhalfofthetestwhen(Z=33.5,N=18,
p<0.05).
Distresswhenseparated

Nointeraction,testordernorepisodeordereffectswerefoundforvocalising,thereforeanalysisfocusedonconditionA,to
minimisetheriskofType1error.ComparisonswithinconditionAofepisodes2and6showedthatcatsvocalisedmoreaftertheir
ownerhaddepartedcomparedtowhenthestrangerdeparted(Z=97.0,N=18,p<0.01),buttherewasnosignificantdifferencein
vocalisationsbetweenA4andA8,whichfollowedthereturnoftheownerorstrangerafteraperiodofisolation.Whenallofthese
episodesarecombinedtoexaminetheoveralleffectofabsenceofownerversusstrangeronvocalisation,therewasnosignificant
difference.
Someofthedatarelatingtoapproaching/orientationtothedoorwerefoundtoexhibitaninteractioneffect(A2vB6,z=88.0,
p<0.05)andsothisparameterwasnotusedtoassessattachment.Thecombineddatarelatingtovigilancehadeitheratestorder
effect(B2+B8vsA6+A4,z=1463.0,p<0.05)oranepisodeordereffect(A2+A8vsB6+B4,z=1178.5,p<0.05)andso
comparisonsofvigilancebehaviourinthesolepresenceoftheownerversusstrangertoassessattachmentwerenotjustifiable,nor
acomparisonbetweentheamountofthisbehaviourineitheroftheseconditionsversuswhenthecatwasalone.Therewere
insufficientdatatoallowstatisticalanalysisoftheparameterrelatingtocontactbythecatwiththeabsentpersonschair.
Discussion

TheaimofthisstudywastouseafullycounterbalancedversionoftheAinsworthStrangeSituationproceduretoexploretheextent
towhichitcanbeusedtoinferthatthecatownerbondconstitutesasecureattachment[9].Overall,theresponseofthecats
indicatedthatthetestenvironmentwasgenerallyadequateforinvokingthetypicalscenariodesiredintheASSTfordemonstration
ofasecurebaseeffect.Howeverthespecificresultsindicatethatmanyaspectsofthebehaviourofcatsinthistestarenot
consistentwiththecharacteristicsofattachment,fortwomainreasons.Firstly,relevantaspectsofthebehaviourofcatsarenot
reliableenoughtobeusedinanevaluationofattachment(i.e.aspectsofthetestproduceunreliabledata).Secondly,evenamong
thosemeasureswhicharetemporallyrobust,thepredictionsarenotmet,exceptinthecaseoflevelofvocalisationifitisaproxyof
distress,butthisaloneisnotsufficienttoimplysecureattachment.Theadditionalcontrolsinthecurrentstudycomparedtothe
previousstudy[7],whichsoughttodeterminewhetherthecatownerrelationshipconstitutedanattachmentasdescribedbyBowlby
[8],[9]explainswhywerejectthishypothesis.Although,weacceptitispossible,ifunlikely,thatthetypicalrelationshipbetween
ownersandtheircatsinMexicoisdifferenttothatwhichgenerallyoccursbetweenownersandtheircatsintheUK.,orthatthereis
adifferenceintherelationshipbetweenownersandcatskeptindoors(whichformedthepopulationtestedbyEdwardsetal.,[7]),
andcatswithoutdooraccess(whichmadeupthemajorityofourpopulation).Wedonotrejectthatcatsmayhavesocial
preferences,northatsomecatsmightformthistypeofattachmentincertaincircumstances,nordowewishtoimplythatcatsdo
notformsomeformofaffectionatesocialrelationshiporbondwiththeirowners(abroadersenseuseofthetermattachment),
onlythattherelationshipwiththeprimarycaregiverisnottypicallycharacterisedbyapreferenceforthatindividualbasedonthem
providingsafetyandsecuritytothecat.AnalternativeexplanationfortheseresultsmightbethatthemodifiedSSTusedhereisnot
anappropriateinstrumentformeasuringattachment,andthefindingthatthebehaviourofcatsappearstobeveryvariable(and
unreliableacrosstime)mayhavewiderimplicationsforthoseusingbehaviouralassessmentstoevaluatecats,suchasfor
rehoming.

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Inrelationtoproximity/contactseeking,manymeasureswerefoundnottoberobustenoughtobeusedtoevaluatethisaspectof
attachment.However,thedataformarking(intheformofbodyrubbing),whichisaspecificbehaviourthatinevitablyresultsin
proximity,wereuseableinthisregarddespiteshowinganepisodeordereffect.Theresultsshowtherewasashiftinthefocusof
markingwithinatest.Earlierinthetest(episodes2&4),catsmarkedthestrangermorethantheownerincomparablesituations
butasthetestprogressedtherewasnopreference(episode6)andfinally(episode8)therewasapreferencefortheowner.This
suggeststhatmarkingpreferenceperseisnotindicativeofattachmenttowardstheindividualbeingmarked,althoughtheseresults
canbeexplainedinanotherway.Ithasrecentlybeensuggested[39]thatmarkingservesanimportantfunctioninrelationto
emotionalarousal,withunfamiliarbutnotovertlythreateningobjectsinitiallybeingmarkedtoreduceanxiousarousalassociated
withtheuncertaintyofthesituation,andfamiliarindividualsmarkedtomaintainthesocialrelationship.Thisallowstheefficient
allocationoflimitedattentionalcapacity.Thishypothesisbuildsonprevioussuggestionsthatthepurposeofmarkingbetweencats
istoexchangeodourssotheybecomefamiliarisedwithoneanother[23],[29],[40]andlaboratorycatshavebeenfoundtomake
moredirectcontactswithanunfamiliarpersonthanwithafamiliarone[41].Theseresultsareconsistentwithanexpansionofthe
familiarisationhypothesisthatincludesasocialpreferencefortheowner,asdescribedbyMillsetal.,[39].Sincethestrangeris
initiallyunfamiliarandnonthreatening,whenthecatisleftalonewiththisindividualforthefirsttime(episode2),duetothe
departureoftheowner,itwouldbeexpectedthatthecatwillmarktheunfamiliarindividualwithwhomitnowfindsitself.Bycontrast
inthecounterbalancedcondition(B),thestrangerhasjustleftandthecatfindsitselfwithitsownerwithwhomitisalreadyis
familiar.Thuswewouldpredictmoremarkingofthestrangerthanownerinthisepisode.Episode4representsthefirstreunionwith
anindividualafterthecathasbeenaloneandgiventheincreasedfamiliarityoftheowner,thesamepredictionapplies.However,as
thetestproceeds,thestrangerisbecomingincreasinglyfamiliartothecat,tothepointthatbyepisode6thedifferencethatexisted
inepisode2islessapparent.Thusinepisode8,whichfollowsthesecondoccasionthecathasbeenleftalone,thereisnow
increasedmarkingoftheowner,perhapsbecausealthoughthetwomaynowbothbefamiliar,theownerisapreferredsocial
contact.Thustheevidencefromproximitymaintenance/contactseekingbythecatinsupportofattachmenttowardsitsowneris
weak.
Thesecurebaseeffectisconsideredtheprimaryfactorinidentifyinganattachment[10],[42].Howevernoevidencewasfoundto
supporttheuseofownersasasecurebaseinthecurrentstudy.Nosignificantdifferencewasfoundintheamountof
exploration/locomotioninthepresenceoftheownerversusstranger,northeamountofplaywiththeownerversusstranger.In
addition,theabsenceoftheownerdidnotsignificantlyreducethetimespentplayingwiththestrangeraswouldbeexpectedifthe
ownerfunctionedasasecurebase[14].Thismightreflecttheobservationthatincats,unlikehumansanddogs,muchplayis
typicallyassociatedwithsolitarypredatorytypeactivity,andsomaynothaveasocialrelevance.Passivebehaviours,indicativeof
relaxation,aresuggestedasameasureofthesecurebaseeffectinchildren[10].However,passivebehaviourmaynotbesoeasy
tointerpretincats[43],[44].Edwardsetal.,(2007)[7]foundthatcatsweremoreinactiveinthepresenceofthestrangerintheir
test,andasimilarresultwasfoundinthecurrentstudy.ThusitseemsthatinthecontextofSST,passivebehaviourbydomestic
cats,maybeassociatedmorewithastateofanxietyratherthancomfort,ashasbeenfoundinotherstudies[43],[44].However,a
differencewasonlyfoundinhalfofthecomparableepisodes,andtheseweretheonesinthemiddleofthetest(episodes4and6).
Iftheownerwereactingasasecurebasewithinthestrangeenvironment,itwouldbepredictedthattheeffectoftheirpresence
overthatofthestrangerwouldbegreatestatthefirstseparation(episode2)butthiswasnotthecase,sincetherewasno
significantdifferenceintheamountofpassivebehaviourexhibitedbythecatatthistime.Atbestitmightbearguedthattheowner
hasasmalleffectontheperceivedsafetyoftheenvironment,andthisisnotstrongenoughtoimpactonthebehaviourofthecat
whenitfirstentersastrangeenvironment,butperhapsasthecathabituatestotheenvironment,theownersmayhaveasmall
effectoverthatofthestranger.However,thiswouldalsoindicatethattowardstheendofthetestthecatwassufficientlyhabituated
totheenvironment,soasnottoneedthesupportofanother.Analternativeandarguablymoreparsimoniousexplanationofthe
findingwouldrelatetothecatsindependenceandhabituationtotheenvironmentandstranger.Thestrangenessofthe
environmentinhibitsthecat(episode2),andthereturnofsomeoneafterthecathasbeenalone(episode4)hasadifferentialeffect
dependingontheidentityofthatindividual.Ifitisthestranger,thenthesituationisstillnovel,whereasifitistheowneritprovidesa
degreeoffamiliarity.Thenextoccasionwhenadifferenceisassessed,isepisode6wheneitherthestrangerorownerleavesafter
theyhavebothbeenpresent.Thelackoffamiliarisationwiththestrangeratthistime,wouldmeantheenvironmentisstillstrange
duetotheirpresence,however,byepisode8(asindicatedbythemarkingbehaviour)thestrangerhasnowbecomefamiliarandso
thereisnodifferencewhenthecatisleftwiththeownercomparedtothestranger.Theseresultsexaminingapotentialsecurebase
effecttogetherwiththoserelatingtoproximityseekingsuggestthereisadynamicbetweenthestrangenessofthephysical
environmentandthestranger,andthathabituationtothemoccursatadifferentrate,occurringtotheenvironmentsoonerthanthe
stranger,withfamiliarisationofthestrangerbeingafunctionofthembeingmarked.
Thedatarelatingtopotentialstresswhenseparatedareconsistentwithapreferenceforinteractionwiththeowneroverthe
stranger,butnotwithsecureattachment.Standingbythedoorisaparticularlyrobustmeasureofseparationdistressindogs[13],
butwasfoundtobeinconsistentincats,aswasvigilancebehaviour.Thissuggestseitherthatcatsdonotshowdistressinthisway,
orthatthecatsarenotparticularlydistressedbythedepartureoftheowner.Bycontrast,vocalisationwasfoundtobearobust
measure,butdifferencesinvocalisationdependingonwhethertheownerorstrangerwasabsent,arenotnecessarilyconsistent
withthebondwiththeownerprovidingasecurebase.Althoughtherewasadifferenceinvocalisationwhenthecatwasleftwith
eithertheownerorstrangeraftertheotherhadleft(episodes6versus8),therewasnodifferenceinvocalisationfollowingthe
returnoftheownerorstrangerafterthecathadbeenalone.Thiswouldbeconsistentwithvocalisationoccurringinresponseto
frustrationattheownersdeparture,perhapsasaresultofpreviousreinforcementoftheinteraction(asoftenoccursatfeeding
[45]),ratherthantheownerprovidingcomfortinthestrangeenvironment.Fromaneurobiologicalperspectiveseparationfroma
secureattachmentfigureresultsinengagementofadifferentaffectivesystem(PANICsensuPanksepp[46]comparedto
separationfromanindividualwhoisassociatedwithphysicalreinforcements(RAGEsensuPanksepp[46]),althoughbothmight
resultinsuperficiallysimilarbehaviouraimedatreinstatingcontact.Inthecaseofthecat,vocalisationmeetstherequirementin
bothsituationsandso,thismeasurealoneisnotsufficienttoinferthatthecatisattachedtoitsownerasasourceofsafetyand
security.
TheAinsworthprocedureissuggestedtobehighlysuitablefordogssinceitreproducessituationsthattheyarelikelytoencounter
intheireverydaylives[14],(potentialneedforsupportfromtheircarer).Incontrastmostcatsareunlikelytoencountersuch
situationsonaregularbasisanditmightbearguedthatthisimpactsnegativelyonthevalidityofthetestasitissuchanartificial
situation.However,inthisparticularinstanceandgiventhetheoreticalunderpinningsoftheSST,wesuggestthatthesetupchosen
actuallyincreasesthevalidityofourprocedureforthefollowingreasons.Thevastmajorityofcatswerehomebasedasiscommon

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intheUKandsoanovelenvironmentislikelytoposeasuitablyintimidatingchallengetoinducetheexpressionofsecure
attachmentrelatedbehavioursiftheyexisted[11].Inaddition,fewofthecatsinthisstudy,hadmuchexperienceofstrange
situationsoutsidethehome.Avisittothevetmightbethemostlikelyanalogoussituationencountered,butnoneweretakentothe
vetregularly(forexamplefortreatmentofachronicmedicalcondition)nonewerereportedtobeexperiencingthistypeofsituation
onaregularbasis.Bycontrast,largelyoutdoorcatswhotravelalottonewplaces,mightgetusedtoenvironmentalnoveltymore
readilyandthiscouldresultinafalsenegativeresponse.Inthisregard,itisworthnotingthatthedatafromtwocatsubjectswere
eliminatedfromtheanalysisbecausetheirbehaviourdidnotshowvariationwithinthetestthehidingandbehaviouralinhibition
observedbythesecatsareconsistentwithhigherstresslevels[43],[44]butitisclearthatthepresenceoftheownerwasnotable
toamelioratetheseeffects,whichshouldbethecaseiftheyserveasanattachmentfigureintheoriginalsenseofBowlby[8],as
comparedtothewidersenseusedbysomeauthors[47].
Itmightbearguedthat,thebehaviourschosentoassessattachmentarenotbiologicallyrelevantgiventhenatureofthecatasa
largelyindependent,solitaryhunter.However,thisaspectofthecatmaybepreciselythereasonwhytherelationshipwiththe
ownerisnotcharacterisedbythesafetyandsecurityfeaturesofaclassicalattachmentbond.Evenwhenaccountingforadifferent
functioninsuperficiallysimilarbehaviourcategoriesbetweenspecies(suchaspassiveness),theevidencefromthecurrentstudy
refutesthenotionthatcatsnormallyshowattachmenttotheownerinthewayBowlbydefinedattachment[8]andhasbeenfoundin
dogs[13]andclaimedtooccurincats[7].Despitethis,thereisgoodevidencethatsomecatscanshowseparationrelated
problems[6]andthereareseveralpossiblereasonsforthis.Itmaybethatasubpopulationofcatsshowingclinicalsignsdo
becomegenuinelyattachedinthewaydescribedbyBowlby,butweconsiderthisunlikelyifattachmenthasastrongbiological
functionandinlightofsomeofourunpublishedobservations.Analternativeexplanationisthattheseproblemsareperhapsmore
ofaresponsetofrustrationatownerabsence[39].Thishypothesislaysthefoundationforfurtherresearchandthedevelopmentof
morespecificinterventionprotocolsasaresult.
Althoughcatscanbesocial,socialityislikelytoexistonacontinuum,varyingbetweenindividuals,butperhapsskewedtowards
independency.Theyhavebeendomesticatedforarelativelyshorttimeincomparisontodogsandhavenotbeenselectivelybredto
liveinclosecontactwithpeople[27],noristheirnaturalsocialsystemhighlydependentonthesametypeofclosesocialbonds
[23].Indeed,withinthehumancatrelationshipthefrequencyanddurationofinteractionshavebeenobservedtobelowin
comparisontodogs[35].Thesefactorsarelikelytoaffectthenatureoftherelationshipthattypicallyformsbetweencatandowner,
andmaketheformationofcathumanattachmentunlikely.Nonetheless,somemaybecapableofformingverystrongattachments,
butthiswouldnotseemtobethenorm.However,catsdoseemtohaveapreferencefortheirowneroveranunfamiliarindividual
buttheextenttowhichthisisconditionedortheresultofanintrinsicpsychologicaltendencytobondremainsunclear.
Conclusion

Itseemsthatgenerallycatsdonotappeartoattachtoownersasafocusofsafetyandsecurityinthesamewaythatdogsdoor
childrendotowardstheirparentsasdemonstratedbytheirbehaviourinastrangesituationtest.However,catsdoappeartohavea
differentrelationshipwiththeirownercomparedtoastranger,buttheextenttowhichthisisconditionedasaresultofincidental
interactionsorbuiltuponthefulfilmentofanintrinsicpsychologicalsocialneedisunknown.
SupportingInformation

S1File.ListofBehaviours.

doi:10.1371/journal.pone.0135109.s001
(PDF)
S2File.Crossoverdesign.

doi:10.1371/journal.pone.0135109.s002
(PDF)
S3File.CrossoverdesignanalysisresultsusingMannWhitney.

doi:10.1371/journal.pone.0135109.s003
(PDF)
Acknowledgments

Theauthorswouldliketoexpresstheirthankstoalltheownersandcatsthatparticipatedinthestudy.ThanksgoalsotoHimara
VanHaevermaetforherassistanceasastranger,andtoLaurenFinkaandSarahEllisfortheircommentsonanearlierdraftofthe
paper,andBarbaraBurgessforherassistancewithdatacollation.
AuthorContributions

Conceivedanddesignedtheexperiments:APDM.Performedtheexperiments:AP.Analyzedthedata:APDM.Contributed
reagents/materials/analysistools:APDM.Wrotethepaper:APDM.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0135109

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