Expression of Behavioural Traits in Goldendoodles and Labradoodles

Abstract

As crossbred dogs gain in popularity, how they express inherited behaviour traits in comparison to their purebred constituent breeds is of interest. We investigated behaviours exhibited by crossbred dogs by focusing on the popular Goldendoodle and Labradoodle crossbreds and comparing them to their corresponding constituent breeds: Standard and Miniature Poodle, Golden Retriever or Labrador Retriever. The data for this study was provided by 5141 volunteer dog owners who filled out the Canine Behavioural Assessment and Research Questionnaire (C-BARQ) online survey. The survey results were used to analyse breed differences in fourteen representative behavioural trait scores: trainability, stranger-directed aggression, owner-directed aggression, dog-directed aggression, dog rivalry, dog-directed fear, stranger-directed fear, non-social fear, touch sensitivity, separation-related problems, excitability, attachment/attention-seeking behaviours, energy and chasing. As expected from a first-generation crossbred (F1), the crossbreds in our study tend to fall between the two constituent parent breeds with some exceptions. Our results suggest that the F1 Labradoodle differed significantly from one of the pure constituent breeds only in dog rivalry, whereas the F1 Goldendoodle behaviour varied from one or more pure constituent breeds in dog rivalry, dog-directed aggression, dog-directed fear, and stranger-directed fear. These results can help advise future dog owners on behavioural trends for particular crossbreds.

Full text

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Animals2019,9,1162;doi:10.3390/ani9121162www.mdpi.com/journal/animals
Article
ExpressionofBehaviouralTraitsinGoldendoodles
andLabradoodles
VictoriaL.Shouldice
1,
*,A.MichelleEdwards
2
,JamesA.Serpell
3
,LeeNiel
4

andJ.AndrewB.Robinson
1

1
CenterforGeneticImprovementofLivestock,DepartmentofAnimalBiosciences,UniversityofGuelph,
50StoneRoadEast,Guelph,ONN1G2W1,Canada;andyr@uoguelph.ca
2
OntarioAgriculturalCollege,UniversityofGuelph,50StoneRoadEast,Guelph,ONN1G2W1,Canada;
edwardsm@uoguelph.ca
3
DepartmentClinicalSciencesandAdvancedMedicine,SchoolofVeterinaryMedicine,
UniversityofPennsylvania,3800SpruceStreet,Philadelphia,PA19104,USA;serpell@vet.upenn.edu
4
DepartmentofPopulationMedicine,UniversityofGuelph,50StoneRoadEast,Guelph,
ONN1G2W1,Canada;niell@uoguelph.ca
*Correspondence:shouldiv@uoguelph.ca
Received:22October2019;Accepted:12December2019;Published:17December2019
SimpleSummary:Crossbreddogsaregaininginpopularitywiththegeneralpublic,butwedonot
fullyunderstandhowthesecrossbredsbehavecomparedtotheirparentbreedsinregardto
inheritedbehaviourtraits.Becauseofthis,weinvestigatedbehavioursexhibitedbycrossbreddogs
byfocusingonthepopularGoldendoodleandLabradoodlecrossbredsbycomparingthemtotheir
correspondingparentorconstituentbreeds:StandardorMiniaturePoodle,andGoldenRetriever
orLabradorRetriever.Thedataforthisstudywasprovidedby5141volunteerdogownersfrom
acrosstheworldwhofilledouttheCanineBehaviouralAssessmentandResearchQuestionnaire(C‐
BARQ)onlinesurvey.Thesurveyresultswereusedtoanalysefourteendifferentrepresentative
behaviouraltraitscores.Asexpectedfromafirst‐generationcrossbred(F1),thecrossbredsinour
studytendtofallbetweenthetwoparentbreedswithsomeexceptions.TheGoldendoodle
displayedmoreproblematicbehaviourwhencomparedtoitsconstituentbreeds,whereasthe
LabradoodleonlydifferssignificantlyfromtheMiniaturePoodleindogrivalry.Theseresultscan
helpadvisefuturedogownersonbehaviouraltrendsforparticularcrossbreds.
Abstract:Ascrossbreddogsgaininpopularity,howtheyexpressinheritedbehaviourtraitsin
comparisontotheirpurebredconstituentbreedsisofinterest.Weinvestigatedbehavioursexhibited
bycrossbreddogsbyfocusingonthepopularGoldendoodleandLabradoodlecrossbredsand
comparingthemtotheircorrespondingconstituentbreeds:StandardandMiniaturePoodle,Golden
RetrieverorLabradorRetriever.Thedataforthisstudywasprovidedby5141volunteerdogowners
whofilledouttheCanineBehaviouralAssessmentandResearchQuestionnaire(C‐BARQ)online
survey.Thesurveyresultswereusedtoanalysebreeddifferencesinfourteenrepresentative
behaviouraltraitscores:trainability,stranger‐directedaggression,owner‐directedaggression,dog‐
directedaggression,dogrivalry,dog‐directedfear,stranger‐directedfear,non‐socialfear,touch
sensitivity,separation‐relatedproblems,excitability,attachment/attention‐seekingbehaviours,
energyandchasing.Asexpectedfromafirst‐generationcrossbred(F1),thecrossbredsinourstudy
tendtofallbetweenthetwoconstituentparentbreedswithsomeexceptions.Ourresultssuggest
thattheF1Labradoodledifferedsignificantlyfromoneofthepureconstituentbreedsonlyindog
rivalry,whereastheF1Goldendoodlebehaviourvariedfromoneormorepureconstituentbreeds
indogrivalry,dog‐directedaggression,dog‐directedfear,andstranger‐directedfear.Theseresults
canhelpadvisefuturedogownersonbehaviouraltrendsforparticularcrossbreds.
Keywords:genetics;cross‐breeding;dogs;behaviour;IGF1;doodles;crossbred;hybrid;C‐BARQ


Animals2019,9,11622of13
1.Introduction
Itisestimatedthattherearecurrentlyover400differentbreedsofdogsaroundtheworld[1].A
breedisaclosedpopulationofcloselyrelatedanimalswhichgenerallyresultsinindividualswith
verysimilarphysicalattributes,relativelypredictablebehaviour,andinsomecasestheselected
abilitytoperformpredeterminedjobs[1–4].Inaddition,thedog‐owningpublicismovingbeyond
thelong‐standingpure‐breedsandembracingcrossbreddogs,withdatabasesofdogbreeds
suggestingthatcrossbreddogsmakeupone‐thirdoftheworld’sdogpopulationandthatthisportion
ofthepopulationisgrowing[5–7].
Itisnotuncommontoencounterapurpose‐bredcrossbreddognowadaysaspeoplearedrawn
moreandmoretodesignerdogbreedsknownasDoodles[8].Doodlesareacrossbetweenapopular
breedsuchasaLabradorRetrieverorGoldenRetrieverandaPoodle[8].Thisisdonewiththeintent
ofproducinganon‐sheddinghypoallergenicdogthatissimilartothenon‐Poodleparent[8].Doodles
arenotnew;theideaofthisgroupofcrossesisoriginallycreditedtoanindividualnamedWally
Conran.WallyworkedfortheRoyalGuideDogAssociationofAustraliainthe1980sandwastrying
tocreateaguidedogthatwasalsohypoallergenic[8].Todothis,hecrossedhisbestbreeding
LabradorwithaPoodle;muchtoWally’ssurpriseheranintoanissuewithpeoplenotwantingto
fosterthecrossbredpuppies[8].Tosolvethis,WallycameupwiththenameLabradoodleand
marketedthiscrossasanewhybriddogbreed[8].Themarketingworkedasthepublicgravitatedto
thisideaofhavingawell‐loveddogbreedthatwashypoallergenicwithoutshedding[8].
Unfortunately,Wallysooncametorealisethatsincethesedogswerehybrids,theydidnothavethe
samepredictabletemperamentormorphologicalaspectsthatpurebredshave[8].Evenso,thepublic
hastakentothesecrossesandtheirpopularityhasgrownsince[8].Doodleshavefollowedpublic
demandandtrendsindogownershipwithmoreandmorecrossesbeingdeveloped,suchasthe
Cockapoo(CockerSpaniel,Poodlecross),Bernadoodle(BerneseMountainDog,Poodlecross),and
Shepadoodle(GermanShepherd,Poodlecross)tonameafew[8].
Itisgenerallybelievedthatcrossbredsarehealthier,havebettertemperaments,andarebetter
all‐arounddogsduetotheabsenceofinbreedingdepression[5,9–11].Purebreddogsareknownto
differbetweenbreedsingeneraltemperamentandpersonalitytraits,andalthoughtherehavebeen
manystudies[1,4–6,12]oftheseinheritedbehavioursinpurebreddogs,thereisstillmuchtobe
understoodaboutthespecificlinksbetweenbehaviourandgenetics[4,5,12].Crossbreedingblends
DNAfromdifferentparentbreeds,andwhiletheinteractionandexpressionofallelesisnotfully
understood[3,4,9,11,13],genetictheorywouldsuggestthatcrossbredsshouldexpressbehaviours
intermediatetothoseoftheconstituentbreeds[14].Whilecrossbreedingisthoughttobeusefulfor
combiningfavourablecharacteristicsfromtwobreeds,littleisknownabouthowtemperamentand
personalitychangeswhencrossingtwopurebreddogs,norhowtheexpressedbehaviourofprogeny
relatestothatoftheparentbreeds[4,5,15].Behaviourexpressionincaninesisnotmeasuredona
binaryscalewhereadogeitherexpressesordoesnotexpressthebehaviourinquestion[4].Instead,
behaviourismeasuredonarelativescaleofexpressionanddogs,eveninpurebreds,willexpressa
setbehaviourtodifferentdegrees[4].Itshouldbenotedthatsomepurpose‐bredbehaviours,suchas
herdingandpointing,willonlybepresentinbreedsthathavebeenselectedtopointorherd.
However,mostnon‐specializeddogbehaviours(e.g.,fear,aggression,trainability,excitability)are
measuredonaspectrumandshowvariabilitybetweenbreeds[1].Duetothenatureofbehaviour
quantificationandourunderstandingofquantitativegenetics[14],wheretheparentbreedsdifferin
scoreforaparticulartrait,itisexpectedthatcrossbreddogswillexpressanintermediatelevelofthe
behaviour[4].Wedefinehereanintermediatelevelofbehaviourexpressionasonethatfallsbetween
thoseoftheconstituentparentbreeds.Fortraitsthatarescoredonascaleofexpression,that
intermediateexpressionwouldbeexpectedtobetheaverageofthescoresoftheparentbreeds.In
thecaseswheretheconstituentparentbreedsdonotdiffersignificantlyfromoneanotherinaverage
behaviourtraitexpressionscore,wewouldexpectthecrossbredstobeconsistentwiththataverage
expressionscoreoftheparentbreedsaswell.Withtheincreaseinpopularityofcrossbreeds,itis
importanttofillthegapsincurrentknowledgetoimproveourunderstandingofthewaysinwhich
crossbreddogtemperamentandpersonalitycomparetothoseoftheirconstituentbreeds.

Animals2019,9,11623of13
Ourobjectivewastoinvestigatebehavioursexhibitedincrossbredsandcomparetheexpression
ofthosebehaviourstotheexpressionofthesamebehavioursbytheconstituentpure‐breeds.Itis
widelybelievedthatanF1hybridshouldinheritpredictablebehaviourasfirstdescribedbyDarwin
[16].WefocusedonLabradoodleandGoldendoodle,whichresultfromcrossingaStandardPoodle
oraMiniaturePoodlewitheitheraLabradorRetrieveroraGoldenRetriever.Asalloftheparent
breeds,includingthepoodles,wereusedforhuntinggamebirds,itisthoughtthatthesedogbreeds
wouldbemoresimilartooneanotherthantonon‐retrieverbreedsandcrosses,suchasthe
Shepadoodle.BecausetheMiniaturePoodleandStandardPoodlearetwodifferentbreedsasdefined
bytheCanadiankennelclub,andsincetheCanineBehaviouralAssessmentandResearch
Questionnaire(C‐BARQ)databasedoesnotaskownersforpedigreeinformation,itwasnecessaryto
comparebothPoodletypestotheDoodlecrosses.Thus,wepredictedthattheLabradoodleand
Goldendoodle,havingparentbreedsfromsimilarworkingbackgrounds,wouldbesimilartotheir
parentbreedswithlittlebehaviouraltendencytowardsoneortheotherparentbreed[15].
Totestthisprediction,weareutilizingtheCanineBehaviouralAssessment&Research
Questionnaire,whichisawell‐validatedquestionnaire‐basedresearchtoolthathasbeenused
extensivelyinpeer‐reviewedstudiesondogbehaviour[17].C‐BARQisanowner‐completed
questionnaireoriginallydevelopedbyYuyingHsuandJamesSerpell[18],thatassesses14different
behaviouraltraitsbasedonquestionsreflectingtheresponsesofdogstovariousreal‐lifescenarios.
Datacollectionhasbeenongoingsince2005,andthecurrentdatabasehasover50,000dog
behaviouralrecordsfromaroundtheworldandincludesover300differentcrossbredsandpurebred
dogs[17,18].Thedatabasewasoriginallycreatedtobeusedforassessingpotentialproblematic
behaviourwithintheworkingandpetdogcommunities[18].Becauseofthelargedatabase,weare
abletocollectphenotypicbehaviouralprofileswhichallowustoassessbehaviouralprofilesofthe
purebredsandDoodlesinourstudyevenintheabsenceofpedigreeinformation.
2.MaterialsandMethods
2.1.DataCollection
ThedataforthisstudyweregeneratedfromvolunteerdogownerswhofilledouttheC‐BARQ
onlinesurveyhostedbytheSchoolofVeterinaryMedicine,UniversityofPennsylvania
(https://vetapps.vet.upenn.edu/cbarq/).TheC‐BARQprojectwaslaunchedin2005andsurveydata
haveaccumulatedsincethattime.DataforthisstudywereextractedandcleanedinApril2019.Data
werecleanedbyremovingidentifiersofownerssuchasemails,non‐completeC‐BARQsurveys,and
dogswithhealthissuessuchashypothyroid,hyperthyroid,Addison’s,severeallergies,oranydogs
withadiseasethatrequiresmedicationsthatmayalterbehaviour.Dogownersareabletocomplete
theC‐BARQsurveyonlineandwereoriginallymadeawareofthesurveyviaveterinaryoffices,dog
trainers,socialmedia,petmagazinesandwordofmouth[17].ThesurveyisorganisedbyownerID
andeachvolunteercancompletethesurveyforuptoamaximumof10dogs.Ownereffectisa
concerninthecurrentdatasetduetotherelativelysmallnumberofcrossbreds,asmulti‐dog
householdscouldpresumablyhavesimilarbehavioursduetoenvironment[18].Wehaveaddressed
theseconcernsinourstatisticalmodel.DuetothenatureoftheC‐BARQproject,wedonothave
pedigreeinformationbutdohaveinformationonwherethedogwasacquired.Wealsohadno
controloverwhofilledoutthesurvey.
2.2.BehaviouralMeasures
Fourteendifferentrepresentativebehaviouraltraitswerepreviouslyextractedbyfactoranalysis
andwereincludedinthisstudy:trainability,stranger‐directedaggression,owner‐directed
aggression,dog‐directedaggression,dogrivalry,dog‐directedfear,stranger‐directedfear,non‐social
fear,touchsensitivity,separation‐relatedproblems,excitability,attachment/attention‐seeking
behaviours,energyandchasing.Thesescoresweredeterminedbyownersratingtheirdogs’
behaviourin100differentscenarios(e.g.,whenapproacheddirectlybyanunfamiliaradultwhile
beingwalked/exercisedonaleash)[18].Eachquestionwasscoredonascalefrom0–4todenotethe

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frequency(0=never;1=seldom;2=sometimes;3=usually;4=always),orseverity(0=nosignsof
thebehaviour;1–3=mildtomoderatesignsofthebehaviour;4=severesignsofthebehaviour)[18].
Fromthere,questionswereorganisedintoeightcategories,threeofwhicharebasedonseverityand
fivebasedonthefrequencyofoccurrence[18].Foreachfactor,scoresfortherelatedquestionswere
combinedtoproduceanaveragescorethatwasusedforanalysis.
2.3.StatisticalAnalyses
SeparateanalyseswerecompletedforLabradoodleandGoldendoodlecrosses.Thus,thetwo
analysesincluded(1)MiniaturePoodle,StandardPoodle,LabradorRetrieverandLabradoodle(LD),
and(2)MiniaturePoodle,StandardPoodle,GoldenRetriever,andGoldendoodle(GD).Therewere
atotalof5141dogsinbothdatasetswith166Labradoodles,2597LabradorRetrievers,157
Goldendoodles,1366GoldenRetrievers,597StandardPoodlesand258MiniaturePoodlesmaking
3618dogsintheLDanalysisand2378dogsintheGDanalysis.Individualdogswereassumedtobe
unrelatedandwedonotknowwhichPoodletypewasusedforeachofthecrossbreddogs.
AllstatisticalanalyseswereperformedusingSASversion9.4;analyseswereconsidered
significantifp≤0.05[19].Outcomevariableswereexaminedusingmixedlinearregressionmodels
usingtheGLIMMIXprocedure.Comparisonswereassessedusingadjustedleast‐squaremeansand
adjusted(usingTukeyKrameradjustment)toaccountfortheunevensamplesizebetweenour
breeds.Thecountrywasincludedinthemodelsasafixedeffect.Thesingletraitlinearanimalmodel
usedintheanalysiswas:
Yijklmnop=μi+breedj+sexk+countryl+whereacquiredm+ageatevaluationn+ownero+ap+eijklmnop
where,
o yijklmnisthebehaviouralobservationforanimalo;
o μistheoverallmeanfortheobservationontraiti;
o breed(j)wasafixedeffect(levelsareequaltoLabradoodle,LabradorRetriever,Goldendoodle,
GoldenRetriever,MiniaturePoodleandStandardPoodle);
o sexisafixedeffect(k,beingeitherfemaleormale);
o countryofresidenceoftheownercompletingthesurveyisafixedeffectrepresentingthe
environmentandculturethedogisfrom;
o whereaquiredisafixedeffectofwhereanowneracquiredtheirdog(m,beingeitherabreeder,
petstore,bredbyowner,shelter,friendorrelative,strayorother);
o ageatevaluationisthefixedeffectoftheageoftheanimalwhenitwasevaluatedintheC‐BARQ
system(n,isthecategoryofthedogs’age;puppy,junior,adult,senior);
o owneristherandomeffectofoonthehouseholdinteraction;
o aistherandomadditivegeneticeffectofanimalp;
o theassumptionsfortherandomeffectsinclude:e ~ N0, Iσ
σ
istheresidualvariance,andI
isanidentitymatrix.
Forallmodels,residualsweretestedforhomogeneityandnormalitybyusingtheShapiro‐Wilk
testandplots.Duetoalackofparentageinformation,inaseparateanalysis,weattemptedtodiscern
thecontributingbreedofPoodleintheLabradoodleandGoldendoodlecrossbredsbyanalysingthe
weightofthecrossbredsrelativetotheweightofthepurebredsusingthe“Procunivariate”function
inSASforallbreedsintheLDandGDanalysis.
3.Results
3.1.Labradoodle
FortheLDanalysis,fourbehaviouralscoresdifferedbetweenbreeds(Table1,Figure1).
LabradorRetrieverandStandardPoodlescoresdidnotdiffersignificantlyfromthoseof
Labradoodlesforanybehaviourcategory.Incontrast,MiniaturePoodlesscoredsignificantlyhigher
thanLabradoodlesfordogrivalry.TheMiniaturePoodlehadahigherscorethantheLabrador

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Retrieverinbothnon‐socialfearandseparation‐relatedproblems,whereastheStandardPoodlehad
alowerscorethantheMiniaturePoodlefortouchsensitivity.Therewereanumberofinteractions
betweenBreedandotherfixedeffects.TheinteractionwithWhereAcquiredwassignificantforallof
themodels,andinteractionswithSex,Country,andAgeatEvaluationweresignificantformostof
themodels.

Figure1.BreedaveragebehaviouralscorescollectedfromC‐BARQfortheLabradorRetrievers,
Labradoodles,StandardPoodlesandMiniaturePoodles.Thetraitsdisplayedabovewerefoundto
havesignificantdifferences(p<0.05)betweenthebreedsintheanalyses.Significantdifferences
betweenbreedsaremarkedwithaandb.abindicatesthatthisbreeddidnotvarysignificantlyfrom
eitherbreedaorbreedb.Behaviouralscoresarerankedfrom0–4,zerobeingneverand4being
always.Errorbarsonthegrapharestandarderror.
3.2.Goldendoodle
TheGDanalysishadsevenbehaviouralscoresthatdifferedbetweenthebreeds(Table2,Figure
2).TheStandardPoodlehadalowerscorethantheGoldenRetrieverforowner‐directedaggression.
TheGoldendoodledifferedfromtheGoldenRetriever,StandardPoodleandMiniaturePoodlein
dog‐directedaggressionwithahigherscorethantheotherthreebreeds.TheMiniaturePoodlehad
thehighestaveragescorefordogrivalryoutofallfourbreedsintheGD.TheGoldendoodlehadthe
highestaveragescorefordog‐directedfearandwassignificantlydifferentthantheStandardPoodle
whichhadthelowestaveragescoreforthistraitoutofallthebreedsinthisanalysis.TheGolden
Retrieverscoredsignificantlylowerforstranger‐directedfearonaveragewhencomparedtothe
Goldendoodle.Ontheotherhand,theGoldendoodledidnotdiffersignificantlyfromtheMiniature
Poodleforaveragescoresforowner‐directedaggression,dog‐directedfear,stranger‐directedfear,
touchsensitivity,andseparation‐relatedproblems.TheMiniaturePoodledifferedfromtheGolden
RetrieverandStandardPoodlewithhigheraveragescoresforbothdogrivalry,andtouchsensitivity.


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Table1.Meanowner‐reportedCanineBehaviouralAssessmentandResearchQuestionnaire(C‐BARQ)scoresformainbehaviouralcategoriesforLabradorRetrievers(n
=2597),Labradoodles(n=166),StandardPoodles(n=597)andMiniaturePoodles(n=258).Modelinteractionsbetweenbreedandotherfixedeffectsarealsoreported.
Breedcomparisonindicateswhenbreedsdiffered.
Trait
ModelEffectBreedMeanBehaviouralScores
BreedBreed×
Sex
Breed×
Country
Breed×Where
Acquired
Breed×Ageat
Evaluation
Labrado
r

RetrieverLabradoodleMiniature
Poodle
Standard
Poodle
Trainability  ● ● ● ● 2.632.732.542.70
Strangeraggression  ● ● ● ● 0.470.560.650.57
Owneraggression ●●● ● ● 0.230.120.320.16
Dogaggression  ● ● ● ● 0.950.620.920.74
DogRivalry●●●●0.44a0.19a1.02b0.37a
Dogfear●●●0.740.900.780.73
StrangerFear●●0.500.690.650.66
Non‐Socialfea
r
 ●  ● ●  0.68a0.91ab1.04b0.72ab
Touchsensitivity ●  ● ●  0.72ab0.76ab1.04a0.59b
Separation‐relatedproblems ●●● ● ● 0.55a0.76ab0.93b0.62ab
Excitability●●2.002.042.281.93
Attachment/attention‐seekingbehaviours  ● ● ● ● 2.042.162.031.98
Chasing    ● ● 1.841.651.861.97
Energy●●●2.112.202.042.07
●Significantdifferencefortheindicatedvariableorinteraction(p<0.05).a,bDifferentletterswithinthesamerowdenotesignificantdifferences(p<0.05).Boldedtextindicatetraits
thatdisplayedsignificantdifferencesbetweenbreeds.


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Table2.Meanowner‐reportedC‐BARQscoresformainbehaviouralcategoriesforGoldenRetrievers(n=1366),Goldendoodles(n=157),StandardPoodles(n=597)and
MiniaturePoodles(n=258.Modelinteractionsbetweenbreedandotherfixedeffectsarealsoreported.Breedcomparisonindicateswhenbreedsdiffered.
Trait
ModelEffectBreedMeanBehaviouralScores
BreedBreed×
Sex
Breed×
Country
Breed×Where
Acquired
Breed×Ageat
EvaluationWeeks
Golden
RetrieverGoldendoodleMiniature
Poodle
Standard
Poodle
Trainability●●2.612.912.542.69
Strangeraggression  ● ● ● ● 0.560.850.670.56
Owneraggression●●●●●0.35a0.19ab0.32ab0.17b
Dogaggression●●●●●0.73a1.68b0.92a0.74a
DogRivalry● ●●●0.42a0.37a1.05b0.38a
Dogfear● ● ●0.82ab1.44a0.79ab0.74b
StrangerFea
r
●●●●●0.48a1.16b0.65ab0.66ab
Non‐Socialfear●●●0.931.121.040.73
Touchsensitivity● ●●●0.65a0.75ab1.04b0.61a
Separation‐relatedproblems●●●●●0.51a0.93ab0.94b0.63ab
Excitability    ● ● 1.972.212.291.94
Attachment/attention‐seekingbehaviours  ● ●   1.892.022.011.98
Chasing●●1.742.231.841.98
Energy●●2.012.052.052.04
●Significantdifferencefortheindicatedvariableorinteraction(p<0.05).a,bDifferentletterswithinthesamerowdenotesignificantdifferences(p<0.05).Boldedtextindicatetraits
thatdisplayedsignificantdifferencesbetweenbreeds.


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
Figure2.BreedaveragebehaviouralscorescollectedfromC‐BARQforGoldenRetrievers,
Goldendoodles,StandardPoodlesandMiniaturePoodles.Thetraitsdisplayedabovewerefoundto
havesignificantdifferences(p<0.05)betweenthebreeds.Significantdifferencesbetweenbreedsare
markedwithaandb.abindicatedthatthisbreeddidnotvarysignificantlyfromeitherbreedaor
breedb.Behaviouralscoresarerankedfrom0–4,zerobeingneverand4beingalways.Errorbarson
thegrapharestandarderror.
Duetothelackofpedigreeinformationinthecurrentstudy,weexaminedthedistributionof
dogweightforboththeLDandGDanalysestodetermineifwecouldpredictMiniatureorStandard
PoodleasthepoodleparentbreedoftheGoldendoodlesorLabradoodles.Theweightsofthe
GoldendoodleandLabradoodlewereevenlydistributedbetweentheStandardandMiniaturePoodle
sodifferentiationofthepoodlebreedinthecrossbredswasnotpossible.
4.Discussion
AstheLabradoodleandGoldendoodleareexpectedtobeF1crosses,onewouldexpectthese
crossbredstodemonstratebehaviouralscorephenotypesthatareintermediatetotheirpurebred
parentbreeds.Thiswasgenerallytrueinthisstudywithsomenotableexceptions.Wefoundthatthe
LabradoodledifferedfromtheMiniaturePoodleforaveragescoreinonlyonetrait,dogrivalry,and
theGoldendoodledifferedfromvariousdifferentparentbreedsforaveragescoreinfourtraits—dog‐
directedaggression,dog‐directedfear,stranger‐directedfear,anddogrivalry.
ThereweresomesimilaritiesacrosstheLDandGDanalyses;forinstance,theMiniaturePoodle
hadthehighestaveragescorefordogrivalryforboththeLDandGDanalyses.Inthisstudy,dog
rivalrywasdefinedas“dogshowsaggressiveorthreateningresponsestootherfamiliardogsinthe
samehousehold”[20].However,rivalrydoesoccurmorefrequentlywithMiniaturePoodlesthanin
theotherpure‐andcross‐breeds,whoseaveragescoresarecloseto“almostnever”frombothLDand
GDanalyses.
Differencesinseparation‐relatedproblemswerenotedinboththeLDandtheGDanalysesas
well,withseparation‐relatedproblemsdefinedas“Dogvocalizesand/orisdestructivewhen

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separatedfromtheowner,oftenaccompaniedorprecededbybehaviouralandautonomicsignsof
anxietyincludingrestlessness,lossofappetite,tremblingandexcessivesalivation.”[18].Inboththe
LDandGDanalyses,theMiniaturePoodlehadthehighestaveragescoreforseparation‐related
problems,andwassignificantlyhigherthantheparentretrieverbreeds,withthecrossbredsshowing
intermediateaveragescoresthatdidnotdiffersignificantlyfromeitherparentstock.Dogswith
higherlevelsofseparation‐relatedproblemshavebeenknowntocauseself‐harmduetoescape
attempts[21].Notonlydoseparation‐relatedproblemshaveanegativeimpactonadog’swelfare,
buttheyalsonegativelyimpactthehuman‐animalbondandinsomecasesleadtorehomingofthe
animal[21].FurtherresearchisneededtodeterminewhetherDoodlesresultingfromMiniature
PoodlecrossesaremorepronetothisbehaviourproblemthanthoseresultingfromStandardPoodle
crosses.
ThelasttraitcommontoboththeLDandGDanalysisistouchsensitivity.Thisasdefinedas
“Dogshowsfearfulorwaryresponsestopotentiallypainfuloruncomfortableprocedures,including
bathing,grooming,nail‐clippingandveterinaryexaminations”.Aswiththeothersimilartraits,the
MiniaturePoodledifferedthemostfromthebreedswithanaveragescoreof1.04.IntheGDanalysis,
theMiniaturePoodledifferedfromboththeGoldenRetrieverandtheStandardPoodle,butinthe
LDanalysis,onlytheStandardPoodledifferedsignificantlyfromtheMiniaturePoodle.
Non‐socialfearistheonlytraitthatshowedsignificantdifferencesintheLDanalysisthatwas
notalsofoundintheGDanalysis.Non‐socialfearisdefinedas“Dogshowsfearfulorwaryresponses
tosuddenorloudnoises(e.g.,thunder,trafficandunfamiliarobjectsandsituations).”TheMiniature
Poodlehadthehighestaveragescoreinthisanalysisandscoredsignificantlyhigherthanthe
LabradorRetriever.Labradoodleshadanintermediateaveragescorebutdidnotdifferfromanyof
theparentbreeds.ThesescoresshowthattheMiniaturePoodledisplayssomenoiseandobject
aversion,whiletheLabradorRetrieverrarelyshowssuchaversion.Thismaysuggestthatthe
MiniaturePoodlehasbeendirectlyorindirectlyselectedtobefurtherremovedfromitsoriginsasa
huntingdogthantheotherpurebreds.Thistrait,likeseparation‐relatedproblems,mayalsohavean
impactonthedog’swelfare,andthereisalsoevidencethatthesetwobehaviouralissueshavean
impactoneachother,asthedogisalreadyinananxiousstatewhentheownerleaves[21].
TheGoldendoodlehadthehighestaveragedog‐directedaggressionscoreintheGDanalysis.
Dog‐directedaggressionwasdefinedas“Dogshowsthreateningoraggressiveresponseswhen
approacheddirectlybyunfamiliardogs”[18].ThiswastheonlytraitintheGDanalysiswherethe
Goldendoodledifferedsignificantlyfromitsconstituentparentbreeds.Theotherbehaviournotedin
theGDanalysiswasOwner‐directedaggressionwhichwasdefinedas“Dogshowsthreateningor
aggressiveresponsestotheownerorothermembersofthehouseholdwhenchallenged,
manhandled,staredat,steppedover,orwhenapproachedwhileinpossessionoffoodorobjects.”
[18].TheGoldenRetrieverhadhigheraveragescoresforowner‐directedaggressionthanthe
Goldendoodle,StandardPoodle,andMiniaturePoodle.
TheGoldendoodleshowedahigheraveragescoreforstranger‐directedfearintheGDanalysis
comparedtothepurebreds,thatwasnotobservedbetweentheLabradoodleandpurebredsinthe
LDanalysis.Stranger‐directedfearisdefinedas“Dogshowsfearfulorwaryresponseswhen
approacheddirectlybyastranger”[18].Formosttraits,theGoldendoodlewasintermediatetothe
parentbreeds,butinthecaseofstranger‐directedfear,theaveragescorefortheGoldendoodlewas
higherthantheGoldenRetriever.ThelastbehaviourthatstoodoutintheGDanalysiswasdog‐
directedfear,astheGoldendoodledifferedsignificantlyfromtheStandardPoodle.The
Goldendoodlehadthehighestaveragescorefordog‐directedfear;comparedtotheGoldenRetriever,
StandardPoodleandMiniaturePoodlewhichallhadmuchlowerscores.Dog‐directedfearwas
definedas“Dogshowsfearfulorwaryresponseswhenapproacheddirectlybyunfamiliardogs.”
[18].
Basedonouranalysesofthepurebredanimalsinthisstudy,theMiniaturePoodledifferedthe
mostfromtheotherpure‐breeds,includingtheStandardPoodle.WealsoobservedtheGoldendoodle
differentiatingfromoneorbothparentbreeds.TheGoldendoodledifferedsignificantlyfromaparent
breedindog‐directedaggression,dog‐directedfear,andstranger‐directedfear.Thesedifferences

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maybelinkedtohybridvigour[1,22,23].Hybridvigourisoneofthereasonsmanyofthepet‐owning
publicacquireaDoodle‐cross;crossbredsareperceivedtobeahealthieranimalsincehybridvigour
hasaproveneffectonfitnesstraitsinotherspeciessuchaslivestock[22].However,wedonotfully
understandtheeffectofhybridvigourinthedomesticateddog,norhowhybridvigouraffects
behaviour[22].AninbreedingstudyconductedbyMellanbyetal.[23]lookedat25differentbreeds,
includingtheGoldenRetrieverandLabradorRetriever.TheauthorsfoundthattheGoldenRetriever
wasoneofthemostinbredbreedsexaminedintheirstudy.Asaresult,theGoldendoodlewouldbe
expectedtohaveagreatereffectofhybridvigourincomparisontotheLabradoodle[22,23]andthus,
potentiallygreaterdifferencesinbehaviourfromtheconstituentbreedsthantheLabradoodle.
ThedifferencesweareobservingintheMiniaturePoodlemaybeduetothecontributionofthe
expressionoftheinsulin‐likeGrowthFactor‐1(IGF1)genewhichaffectsthegrowthandstatureofthe
dog.IGF1isexpressedinmanytoyorminiaturebreedsbutisrareinlargebreeds[1,24,25].
Interestingly,studieshavefoundthattherearesignificantlylowerlevelsofcirculatingIGF1inthe
serumofMiniaturePoodlesincomparisontotheStandardPoodle[1,26–28].Someevidenceshows
thatnotonlyisthisgeneassociatedwithgrowth,butitisbelievedtobelinkedtotemperamentas
well[1,24,29].AstudyconductedbyUhdeandcolleagues[29]bredGermanShorthairedPointersfor
fearfulornervousbehaviour,andtheyfoundaninverselinearcorrelationbetweenfearfulbehaviour
andtheexpressionofIGF1.ThissuggeststhatlowerlevelsofIGF1expressionmakesmallerdogs
morefearful,reactive,excitable,andsensitivetotouch[1,24,29].Withoutpedigreeinformation,we
unfortunately,cannotknowifthereisanydifferenceinbehavioursbetweenDoodlescrossedwitha
MiniaturePoodleorStandardPoodle;however,ourresultssuggesttheremaybesomedifferential
expressionofIGF1occurring.Forinstance,weobservedthattheMiniaturePoodledifferedfromthe
otherpurebreddogsindogrivalry,non‐socialfear,touchsensitivity,separation‐relatedproblems,
dog‐directedaggression,stranger‐directedfear,anddog‐directedfear,whichareallbehaviours
consideredtobehigheramongsmallbreedsandcouldberelatedtoexpressionofIGF1[1,24,29].
ThesebehavioursthatmaybeassociatedwithIGF1expressionarethesamebehavioursinourstudy
thatwesawsignificantaveragescoredifferencesbetweentheLDandGDanalyses.IftheIGF1gene
doesinfluencefearandaggression,itcouldcreatewelfareimplicationsforthedogswiththisgene
expression.Fearisanegativeaffectivestatethatcanimpairanimalwelfare,particularlywhenit
occursathighlevelsandisprotracted[12,21,27].Itcanalsoleadtoaggressionandotherbehaviour
problemsthatresultinabreakdownofthehuman‐animalbondandincreasethelikelihoodof
euthanasiaorrelinquishment[12,21].Basedonourscoresfordog‐directedaggressionanddog‐
directedfearbehavioursintheGoldendoodle,itwouldappearthiscrossexpresseselevatedlevelsof
aggressionandfear‐basedbehaviours,andthattheseissuesarenotpresentintheLabradoodle.
Althoughtheaveragescoresobservedinthecurrentstudyarerelativelylowoverall,itisimportant
thatownersareawareofpotentialimpactsondogbehaviourandwelfare[12,21,27].
PreviousresearchhasfoundthattheLabradorandGoldenRetrievershavecomparativelylow
occurrencesofaggressivebehaviours[17].Incontrasttothesepredictionsaboutoneoftheir
constituentparentbreeds,weobservedelevatedlevelsofdog‐directedaggressionfromthe
Goldendoodle,andwealsosawhigherlevelsofdog‐directedfearandstranger‐directedfear.This
correspondstowhatotherstudieshavefoundwhenexaminingIGF1expressionandcrossbreddogs
[7,26,28,29].BennettandRholf[7]examinedcrossbreddogsandfoundthemtobemorefearful,
aggressive,vocalandneuroticwhencomparedtopurebreddogs.Temesiandcolleagues’[30]study
alsoagreedwithBennettandRholfs’[7]findingsastheytoonotedneuroticism,dog‐directedfear,
andhuman‐directedfearincross‐breeds.Similarly,HsuandSun[31]foundthatmixedbreeddogs,
ingeneral,seemtohaveahigherexpressionofaggressionandfear‐basedbehaviours.Thisdifference
incrossbredscouldbeattributableinparttoheterosis,althoughthesestudiesdidnotdifferentiate
betweenF1hybridssuchastheGoldendoodleandLabradoodleandmixedbreedsofunknown
origins[4,22,23].Retainedheterosismaybelowerinmixedmulti‐breeddogscomparedtoheterosis
inF1crosses[4]
WhiletheinfluenceoftheIGF1geneisonepotentialexplanationforthebehaviouraldifferences
observedinMiniaturePoodles,behaviourinthesedogsmightalsohavebeeninfluencedby

Animals2019,9,116211of13
differencesinthewaysthatsmallandlargedogsaretreatedbyowners.Arhantandcolleagues[32]
foundthatthesizeofadoghasanimpactonhowdogownersinteractwiththeanimalandthat
smallerdogsweremorelikelytohaveunfavourablebehaviours,suchasdisobedience,increased
aggression,excitabilityandfearfuloranxiousbehaviours[32–35].Theauthorssuggestedthis
differenceisdueinparttohowownersofsmalldogsinteractwiththeiranimals,withownersof
smalldogsshowingmoreinconsistencyintheirinteractions,andreportinglowerlevelsoftraining,
exerciseandhuman‐dogplaybehaviour[34–36].Poorbehaviourfromsmallerdogsisalsotolerated
betterbythepublic,asdemonstratedbystatisticsondogbiteoccurrence[34,35].Onaverage,smaller
breeddogsbitemorefrequentlyandleavelacerationsontheirhumanbitevictims,whilelargerbreed
dogsdonotbiteasoftenassmallerdogsbutcreatemoredamage[34].Becauseofthis,largerdogs
thathavebrokenskinaremuchmorelikelytobeeuthanizedduetoaggressivebehaviourthan
smallerdogsthatdisplaythesamebehaviourbutcreatelessdamage[34].Ownerlifestyle,
demographics,ethnicityandlivinglocationmayalsoplayaroleinhowsmalldogownersinteract
withtheirdog[34].Becauseofthistolerancetowardspoorbehaviourinsmallerdogs,itwouldnot
besurprisingthatlessselectionagainstpoorbehaviourmayoccurinsmallbreeddogs[34,35].There
isalsoevidencethatsuggestsbodysize,weightandskullshapemayhaveanimpactondifferent
behaviourswhichmayprovidesomeexplanationforthevariationobservedbetweenthelargeand
smallpurebredsincludedinthecurrentstudy[35].Furtherresearchisneededtodeterminewhether
thetypeofPoodlethatisusedinthecross‐influencesthebehaviourofDoodlebreeds.
Aswithallresearch,thisstudyhascertainlimitationsthatmighthaveinfluencedthefindings
andconclusions.Theremaybesomebreedidentificationerrorsinthedataforthedogsincludedin
thecurrentstudy;C‐BARQrecordsarebasedonownerreports,thus,bothpurebredsandcross‐
breedsmightbemisclassifiedbyowners.Forthesamereason,wealsodonotknowhowrelatedthe
dogsinthestudyareoriftheyarefromthesamebreederororigin.Ownerinformationwas
accountedfor,andwehaveassumednorelationshipbetweendogsandthatallcrossesareF1crosses.
Inaddition,wehadarelativelysmallsamplesizeofcrossbreddogswhencomparedtoourpurebred
animals,whichmayimpactthegeneralisabilityofourresults,inspiteoftheTukey‐Kramer
adjustmentusedtoaccountforunbalanceddata
5.Conclusions
AsexpectedfromanF1cross,thecross‐breedstendedtoexpressintermediatebehaviour
betweenthetwoconstituentpure‐breedswithsomeexceptions.TheGDanalysisshowedthemost
differencebetweentheconstituentpure‐breeds.Evenwiththesedifferences,theGoldendoodleonly
differedsignificantlyfromoneormoreoftheparent‐breedsindog‐directedaggression,dog‐directed
fear,stranger‐directedfear,anddogrivalry.ThecrossbredintheLDanalysisshowedthefewest
behaviouraldifferencesfromtheotherparent‐breedswiththeexceptionofdogrivalry,butthatwas
duetotheMiniaturePoodledifferingfromtheotherbreedsintheLDanalysis.Theseresultssuggest
thatdifferentialexpressionoftheretriever‐basedbehaviouraltendenciesisdependentonthe
retrieverorigin.FurtherresearchisneededtodeterminewhetherIGF1expressionmightplayarole
inbehaviouraltendenciesforpoodlecrosses,andhowthisisinfluencedbycontributionsfromthe
non‐poodleparent.Overall,theresultsofthecurrentstudycanassistbreedersandownersin
predictinglikelybehaviouralphenotypesforLDandGDcrossbreds,andthisinformationcanbe
usedtoassistownersinselectingbreedsthatbestfittheirneedsandexpectations.
AuthorContributions:Conceptualization,V.L.S.,L.N.,J.A.S.andJ.A.B.R.;methodology,V.L.S.,L.N.and
J.A.B.R.;software,V.L.S.,L.N.,A.M.E.andJ.A.B.R.;formalanalysis,V.L.S.,L.N.,A.M.E.andJ.A.B.R.;data
curation,J.A.S.;writing—originaldraftpreparation,V.L.S.;writing—reviewandediting,V.L.S.,L.N.,J.A.S.,
M.E.andJ.A.B.R.
Funding:Thisresearchreceivednoexternalfunding.
ConflictsofInterest:Theauthorsdeclarenoconflictofinterest.


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