Assessment of Body Condition in African (Loxodonta africana)

20 Pages·2016·3.86 MB·English

RESEARCHARTICLE
Assessment of Body Condition in African
Loxodonta africana Elephas
( ) and Asian (
maximus
) Elephants in North American Zoos
and Management Practices Associated with
High Body Condition Scores
KariA.Morfeld1,2*,CherylL.Meehan3,JenniferN.Hogan3,JanineL.Brown2
a11111
1 LincolnChildren’sZoo,Lincoln,Nebraska,UnitedStatesofAmerica,2 CenterforSpeciesSurvival,
SmithsonianConservationBiologyInstitute,SmithsonianNationalZoologicalPark,FrontRoyal,Virginia,
UnitedStatesofAmerica,3 AWAREInstitute,Portland,Oregon,UnitedStatesofAmerica
*[email protected]
OPENACCESS
Abstract
Citation:MorfeldKA,MeehanCL,HoganJN,Brown
JL(2016)AssessmentofBodyConditioninAfrican Obesityhasanegativeeffectonhealthandwelfareofmanyspecies,andhasbeenspecu-
(Loxodontaafricana)andAsian(Elephasmaximus)
latedtobeaproblemforzooelephants.Toaddressthisconcern,weassessedthebody
ElephantsinNorthAmericanZoosandManagement
PracticesAssociatedwithHighBodyCondition conditionof240elephantshousedinNorthAmericanzoosbasedonasetofstandardized
Scores.PLoSONE11(7):e0155146.doi:10.1371/ photographsusinga5-pointBodyConditionScoreindex(1=thinnest;5=fattest).Amulti-
journal.pone.0155146
variableregressionanalysiswasthenusedtodeterminehowdemographic,management,
Editor:SadieJaneRyan,UniversityofFlorida, housing,andsocialfactorswereassociatedwithanelevatedbodyconditionscorein132
UNITEDSTATES
African(Loxodontaafricana)and108Asian(Elephasmaximus)elephants.Thehighest
Received:May22,2015 BCSof5,suggestiveofobesity,wasobservedin34%ofzooelephants.Inbothspecies,
Accepted:April23,2016 themajorityofelephantshadelevatedBCS,with74%intheBCS4(40%)and5(34%)cate-
gories.Only22%ofelephantshadBCS3,andlessthan5%ofthepopulationwasassigned
Published:July14,2016
thelowestBCScategories(BCS1and2).Thestrongestmulti-variablemodeldemonstrated
Copyright:Thisisanopenaccessarticle,freeofall
thatstaff-directedwalkingexerciseof14hoursormoreperweekandhighlyunpredictable
copyright,andmaybefreelyreproduced,distributed,
transmitted,modified,builtupon,orotherwiseused feedingscheduleswereassociatedwithdecreasedriskofBCS4or5,whileincreased
byanyoneforanylawfulpurpose.Theworkismade diversityinfeedingmethodsandbeingfemalewasassociatedwithincreasedriskofBCS4
availableundertheCreativeCommonsCC0public
or5.OurdatasuggestthathighbodyconditionisprevalentamongNorthAmericanzooele-
domaindedication.
phants,andmanagementstrategiesthathelppreventandmitigateobesitymayleadto
DataAvailabilityStatement:Forreasonsrelatingto
improvementsinwelfareofzooelephants.
protectionofthefacilitiesandanimalsincludedinthis
study,accessrestrictionsapplytotheindividual-level
dataunderlyingthefindings.Adatasetofde-
identified,population-leveldataisavailableatdoi:10.
6084/m9.figshare.3383554.
Funding:Fundingforthisworkwasprovidedbya Introduction
NationalLeadershipGranttotheHonoluluZoological
Obesityisasignificanthealthproblemforhumans[1–3],companionanimals,[4–6]andlive-
SocietyfromtheInstituteofMuseumandLibrary
stock[7,8].Likewise,thereisgrowingconcernaboutthehealthofzooanimalsasitrelatesto
Services(www.imls.gov)grantnumber:LG-25-10-
0033-10.Employersprovidedfinancialsupportinthe obesityandrelatedconditions[9–12].Inelephants,obesityhasbeenspeculatedtobea
PLOSONE|DOI:10.1371/journal.pone.0155146 July14,2016 1/20
BodyConditionofZooElephants
formofauthors'salariesasfollows:Smithsonian problembecauseofplausibleassociationswithconditionsthreateninghealthandpopulation
NationalZoologicalPark(JLB,KM);Lincoln sustainability,suchascardiovasculardisease,arthritisandfootproblems,andovariancycle
Children’sZoo(KM).AftertheIMLS-fundedperiodof abnormalities[10,12,13–19].
performance(November2010–December2013)
Obesityisdefinedasanaccumulationofexcessiveamountsofadiposetissue(fat)inthe
AWAREInstituteprovidedsupportintheformof
salariesforauthorCMandJH.Thespecificrolesof body[20].Allmeasuresofadiposityinvolvedefiningbodycomposition,ortherelative
theseauthorsarearticulatedinthe‘author amountsoffatversusleanbodymass.Varioustechniquesareavailabletomeasurebodycondi-
contributions’section.Neitherthefundersnor tion,andthesedifferinapplicabilityaccordingtothespeciesofinterestandthecontextofthe
authors’employershadanyroleinstudydesign,data assessment.Forexample,criteriahavebeenestablishedforwhatconstitutes“overweight”and
collectionandanalysis,decisiontopublish,or “obese”inhumans,andareusuallybasedonmeasuresofadiposity,suchasbodymassindex
preparationofthemanuscript.
(BMI)(weightdividedbyheight2)usingepidemiologicalmethods.Dogsandcatsareclassified
CompetingInterests:JLBandKMareemployedby asoverweightwhentheirbodyweightis>15%abovethedefinednormalforthespecies,and
SmithsonianNationalZoologicalPark(anAZA-
asobesewhentheirbodyweightexceeds30%oftheoptimalweight[20].
accreditedzoo).AuthorKMwasemployedbyLincoln
Children’sZoo(anAZA-accreditedzoo)atthetimeof Abodyconditionscore(BCS)estimatesadipositybasedonvisualortactileevaluationsof
thestudy.CMandJHareemployedbyAWARE muscletoneandkeyskeletalelements[20–21].Anumberofscoringsystemshavebeendevel-
Institute.AWAREInstituteisacommercialentity opedforavarietyofspecies,andscoresarecommonlybasedonanordinal5-or9-pointscale
foundedbyCMin2014andprovidesanimalwelfare [20,22].Lowscoresrepresentanimalswithlessbodyfat,whereashigherscoresrepresentani-
assessment,researchandeducationservicesto
malswithmorebodyfat.Forexample,twonumericscalesaretypicallyusedandacceptedin
zoosandaquariums.Theseinterestsdonotalterthe
veterinarypracticesforassessingbodyconditionindogs(5-ptand9-ptscales)[23,24].When
authors'adherencetoallthePLOSONEpolicieson
sharingdataandmaterials,asdetailedonlineinthe usinga5-pointscale,the“ideal/normal”BCS=3,BCS=1–2equatesto“underweight/thin”
guideforauthors. and“overweight/obese”includesBCS=4–5.Whenusinga9-pointscale,the“ideal/normal”
BCS=4–5,whereas“underweight/thin”isrepresentedbyBCS=1–3and“overweight/obese”
includeBCS=6–9.Similarly,incattle,both9-point[25,26]and5-point[27,28]scalesare
used,andthemiddlescoresrepresentthe“ideal/normal”distributionofbodyfat.Insome
cases,thesevisualscaleswerevalidatedusingadditionalbiologicalmeasuresofadiposity.For
example,ultrasoundmeasuresofactualfatthicknesshavebeenusedtovalidateBCSmethods
inanumberofdomesticandnon-domesticspecies,includingcattle[22],moose(Alcesalces)
[29],elk(Cervuselaphus)[30],woodlandcaribou(Rangifertaranduscaribou)[31],pinnepeds
[32],andAfricanelephants(Loxodontaafricana)[19].Physiologicalmeasuresofadiposity
havealsobeenusedforvalidatingvisualscales.Forexample,serumtriglycerides,whichare
storedinadiposetissueandinvolvedinfatdeposition[33,34],werefoundtocorrelatewith
visuallyassessedbodyconditionscoresintigersharks[35]anddogs[36].Inaddition,leptin,
whichissynthesizedandsecretedprimarilybyadipocytes[37],hasbeenshowntopositively
correlatewithbodyconditionscoresinrodents[38],horses[39],anddogs[40,41].Bodycon-
ditionscoringsystemsareroutinelyusedinthemanagementandcareofmanyspecies,includ-
inghorses,cattle,sheep,mice,anddogs[42,43],whereBCSateitherendofthescale(i.e.,very
thinorveryfat)canindicatecompromisedwelfare.Forexample,emaciationorlowBCSmay
resultfrominadequatefeedintake,inappropriatenutrition,chronicdisease,poordentalcare,
orparasitism[44,45].Attheotherextreme,highBCS(i.e.obesity),aproblemspeculatedfor
zooelephants[10,12,13–19],maybeaconcernduetothehostofsecondarydiseasesthatcan
accompanyadiposity.
Theprincipalcauseofobesityinanyspeciesisanenergyimbalance,wherecaloricintake
exceedsenergeticexpenditure.Inhumans,theriskfactorsassociatedwithobesityhavebeen
thoroughlyinvestigatedandincludeavarietyoflifestyle,environmental,andgeneticfactors
[46–48].Althoughanumberoffactorswithinthezooenvironmentarelikelytoinfluencebody
conditioninelephants,thereisapaucityofliteraturethatscientificallyinvestigateselephant
obesityandassociatedriskfactors.Therefore,theobjectivesofthisstudywereto1)determine
thedistributionofbodyconditionscoresofelephantsinaccreditedNorthAmericanzoosfor
thefullpopulationandbyspeciesandsex,and2)usemulti-variableregressionmodelingto
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determinethedemographic,management,housing,andsocialfactorsassociatedwith
increasedriskofelephantsbeingclassifiedasoverweightorobese.
The5-pointvisualindexusedforassessingbodyconditioninAfricanelephantswasprevi-
ouslydevelopedandvalidatedwithultrasoundmeasuresofsubcutaneousfatbyMorfeldetal.
[19].Inthepresentstudy,asimilarBCSindexforAsianelephantswasdevelopedandtested
forinter-assessorreliabilityandbiologicalvalidity.Ourstudyisthefirstlarge-scaleinvestiga-
tionofelephantbodyconditionandwasacomponentofalargerstudyentitled“UsingScience
toUnderstandZooElephantWelfare”,amulti-institutionalcollaborativeefforttoproducesci-
entificdatatosupportdecisionmakingwithregardtobestpracticesinelephantmanagement
[49].
MaterialsandMethods
EthicsStatement
Alldataincludedinthisstudyweresourcedfromelephantprogramsat65zoosaccreditedby
theAssociationofZoosandAquariums(AZA)andanimalsenrolledintheUsingScienceto
UnderstandZooElephantWelfarestudy[49].ThesezooswerelocatedintheUnitedStates,
MexicoandCanada.Bothzoo-levelandelephant-leveldatawerecollected.Thisstudywas
authorizedbythemanagementateachparticipatingzooand,whereapplicable,wasreviewed
andapprovedbyzooresearchcommittees.Inadditionthestudyprotocolwasreviewedand
approvedbytheZoologicalSocietyofSanDiegoInstitutionalAnimalCareandUseCommittee
N.I.H.AssuranceA3675-01;Protocol11–203.
DevelopmentandTestingoftheAsianElephantBodyConditionScoring
Index
TodeveloptheAsianBCSindex,avarietyofphotographsofelephantswereevaluatedtoiden-
tifykeybodyareasthatwouldserveastheanatomicalregionsforassessingbodyfatdeposition
patterns(ribs,pelvis,backbone:seeFig1).Photographsofbothofzooandfree-rangingAsian
Fig1.KeyareasforassessingBCSinAsianelephants.
doi:10.1371/journal.pone.0155146.g001
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elephantswereusedtoincludethepossiblerangeofbodyconditions(thinnesttofattest)for
thespecies.SimilartodevelopmentoftheAfricanelephantBCSindex[19],comparisonswere
madeamongseveralphotographsandeachbodyregionwasassessedforphysicalevidencethat
demonstrateddifferencesinfatdeposition.Thesedifferenceswerethencategorizedinorderof
severitysuchthatuniquephysicalcharacteristicscouldbeassignedtoeachtoeachBCScate-
gory(seeFig2).Forexample,forBCS5,thebackboneisnotvisibleandfatfillstheregion
alongsidetheentirelengthofthebackbone,givingaroundappearance.Withlessfatdeposi-
tion,thespinousprocessesofthevertebraappearmakingthebackbonevisibleforBCS4.The
vertebraareprogressivelymorevisiblemakingthebackbonemorepronouncedforBCS3,
althoughsomefatisstillvisiblealongsidethebackbone.Inthinelephants(BCS1and2),the
depressionalongsidethebackbonebecomesobviousduetominimalfataccumulationinthis
regionandthebackboneisvisiblefromtailheadtoshoulders.
Todetermineinter-assessorreliabilityoftheAsianBCSindex,threeassessorsscored40sets
ofphotographs(sideview,rear-angleview,andrearview)fromthestudypopulation.Raters
includedtheleadauthorwhodevelopedtheBCSindex(AssessorA),anundergraduatestudent
majoringinBiology(AssessorB),andapre-veterinarystudent(AssessorC).AssessorsBandC
hadnopriorexperienceinscoringbodyconditionofanyspeciesandwereblindedtothestudy
objectives.Assessorsindependentlyscoredthephotographs.
FortheAsianBCSindexbiologicalvalidation,bloodsampleswerecollectedbyon-sitestaff
withoutanesthesiafromeitheranearorlegvein.Protocolsrequestedblooddrawstooccur
before12noon.Bloodwasmaintainedat~4°C,allowedtoclotatroomtemperature,thencen-
trifugedat~1500gfor~20min.andtheserumstoredat-20°Corcolderuntilanalysis.Triglyc-
eridelevelswereassessedusingaDimensionsXPandIntegratedPlusChemistrySystem
(SiemensHealthcareDiagnostics,Inc.,NewYork,USA)generalchemistrypanel.
BodyConditionAssessment
Zooswereprovidedaphotographicguidecontainingdetailedinstructionsonhowtoobtain
threestandardizedphotosforeachelephantforvisualbodyconditionassessment.Elephants
withcompleteandaccuratesetsofphotographswereincludedintheanalysisandallphoto-
graphswereanonymizedandscoredbyK.Morfeldusingtheappropriatespecies-specificBCS
index.
EpidemiologicalAnalysis
Independentvariableswereselectedbasedonhypothesesregardingtheirpotentialassociation
withBCS.Definitionsfortheindependentvariablesselectedfortestinginthisstudyare
describedinTable1.Detailsonthecollectionandcalculationofindependentvariablesarepre-
sentedbyMeehanetal.[50],Prado-Oviedoetal.[51],andGrecoetal.[52].
Twoadjustmentsweremadetoindependentvariablesfromtheiroriginalformat.TheSpace
Experiencevariables[50]wereadjustedtoavalueof“per500ft2”toaidininterpretationof
Betavalues.FeedingPredictabilityoriginallyconsistedofthreecategories[52]:“predictable”
(feedingtimeswereconsistentfromdaytoday),“semi-predictable”(feedingtimeswereinten-
tionallyvariedbyupto60minfromdaytoday),and“unpredictable/random”(feedingtimes
werenotscheduledoroccurredrandomly).Toaccountforsamplesizelimitations,Feeding
Predictabilitywasconvertedtoabinaryvariable:predictableandsemi-predictablewerecom-
binedandclassifiedas“predictableschedule”andusedasthereferencecategoryinwhichto
assesstheeffectoftheunpredictable/randomschedule.
TheBCS=3wasdesignatedasthereferencescorebasedontheinterpretationofBCS
indexesusedandacceptedinveterinarymedicine,inwhichthemiddlescorerepresentsthe
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Fig2.Bodyconditionscoring(BCS)indexforAsianelephants.
doi:10.1371/journal.pone.0155146.g002
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Table1. DescriptionofstudyvariablesforassessingassociationswithbodyconditionscoreinAsianandAfricanelephants.
Variablea Unitof Description
Analysis
Demographics1
Age Elephant Ageofelephant(years)
Sex Elephant Femaleormale
Species Elephant AfricanorAsian
Origin Elephant Captiveorwildborn
Exercise2
ExerciseWeek Elephant Numberofreportedhoursspentexercisinganimalseachweek;rangingfrom1(<1hourperweek)to7(14
ormorehoursperweek)
WalkWeek Elephant Numberofreportedhoursspentwalkingelephantseachweek;rangingfrom1(<1hourperweek)to7(14
ormorehoursperweek)
Feeding2
FeedDay Zoo Numberoffeedingsduringtheday
FeedNight Zoo Numberoffeedingsduringthenight
FeedTotal Zoo Sumoffeedingsduringthedayandnight
FeedingPredictability Zoo Thepredictabilityoffeedingactivities;1=predictable:feedingtimesconsistent,andmayintentionallyvary
byupto60min,fromdaytoday,and2=unpredictable:feedingtimesarenotscheduledandoccur
randomly
FeedingDiversity Zoo Shannondiversityindexofthenumberoffeedingtypesandfrequencywithwhicheachtypewasprovided
Spread Zoo Relativefrequencyofthepercentageoftimefoodwasspreadaroundtheexhibitcomparedtoallfeeding
techniques
AlternativeFeedingMethods Zoo Relativefrequencyofthepercentageoftimefoodwaspresentedinaforagingdevice,hidden,orhanging
comparedtoallfeedingtypes
Housing3
PercentTimeIndoor Elephant Percenttimespentinindoorenvironments
PercentTimeIn/OutChoice Elephant Percenttimespentinenvironmentswithanindoor/outdoorchoice
SpaceExperience Elephant Theaverageweighted(bypercenttime)sizeofallenvironmentsinwhichanelephantspenttime.
SpaceExperienceper Elephant Theaverageweighted(bypercenttime)sizeofallenvironmentsinwhichanelephantspenttimedividedby
Elephant thenumberofelephantssharingtheenvironment.
Social3
AnimalContact Elephant Maximumnumberofuniqueelephantsfocalanimalisincontactwith
SocialGroupContact Elephant Maximumnumberofuniquesocialgroupsfocalanimalispartof
TrainingandEnrichment2
RewardingStimuli Elephant Percenttimewithwhichanelephantexperiencedtechniquesinvolvingtheprovisionorremovalof
TechniquesScore rewardingstimulidividedbythepercenttimealltrainingtechniqueswereexperienced;rangingfrom1
(never)to9(veryfrequently)
EnrichmentDiversity Zoo Shannondiversityindexofthenumberofenrichmenttypesandfrequencywithwhichtheywereprovided
aReferencesforvariabledevelopmentanddescription:1.Prado-Oviedoetal.[51];2.Grecoetal.[52];3.Meehanetal.[50].
doi:10.1371/journal.pone.0155146.t001
“ideal/normal”distributionofbodyfat[23–28].Thisdesignation(BCS3=ideal/normal)is
alsoutilizedintheAfricanelephantindex[19],soutilizingthesamescalingterminologyallows
forconsistencyacrossthetwoelephantspecies.
StatisticalAnalysis
Frequencyofbodyconditionscores(1,2,3,4,and5)werecalculatedforthefullpopulation,by
sex,andbyspecies.TherelationshipbetweenBCSandtriglyceridelevelswasinvestigated
usingone-wayanalysisofvariance(ANOVA)procedureswithScheffé’stestasaposthocfor
pairwisecomparisonsofsubgroups.
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Tocalculatetheinter-assessorreliabilityfortheAsianBCSindex,theoverallpercentage(%)
agreementbetweeninter-assessorassessmentswascalculatedas(100×m)/n,wheren=total
numberofsamplesexaminedandm=numberofcasesofexactagreement.Aweightedkappa
(κ )statisticwasalsousedtoanalyzeinter-assessorvariability[53].Standardsproposedby
w
LanidisandKoch[54]wereusedtointerpretresultingkappavalues,whereperfectagreement
equatestoakappaof1andchanceagreementequatesto0.Thefollowingstandardsforinter-
pretingkappavaluesforstrengthofagreementwereused:kappavalues(cid:1)0=poor,0.10to
0.20=slight,0.21to0.40=fair,0.41to0.60=moderate,0.61to0.80=substantialand0.81to
1.00=almostperfectagreement.
Avarietyofdemographic,management,housing,andsocialcharacteristicswereevaluated
asriskfactorsforassociationswithincreasedBCS(Table1).PredictivemodelsforBCSwere
fittedusinggeneralizedestimatingequations(GEE),whichallowsforrepeatedmeasurement
andclusteringofindividualanimalswithinzoos[55–57].Zoosweretreatedasrandomeffects
andanindependentcorrelationstructurewasspecified[57].BCS3wassetasthereference
levelandmultinomiallogisticregressionwasusedtodetermineriskfactorsassociatedwith
increasedBCSwhereBCS4wascomparedto3andBCS5wascomparedto3.Multi-variable
regressionmodelswerebuiltbyfirstassessingindividualpredictorsattheunivariateleveland
thenatthebivariatelevelwithdemographicvariablesdeterminedtobepotentialconfounders
(age,sex,species,andorigin)[58,59].Confoundingvariableswereincludedinallmodelsand
anyvariablesthatwereassociatedwithriskofincreasedBCSatPvalue<0.15intheunivariate
orbivariateassessmentswereretainedforevaluationinthehierarchicalmodelbuilding
process.
Onceasetofviableinputvariablesandconfounderswasidentified,thehierarchicalmodel
buildingprocessproceededusingtheforwardselectionapproach[60].Modelsreachingthe
multi-collinearitycriteria,asdefinedbyavarianceinflationfactorofgreaterthan10andacon-
ditionindexofgreaterthan30,werenotconsideredforfurtheranalysis[60].Theforward
selectionofvariableswascontinueduntiltheadditionofvariablesnolongerresultedinsignifi-
cantmodels.Thefinalmodelwasselectedbasedonquasi-likelihoodundertheindependence
modelcriterion(QIC)values[61]andparameterestimatesofexplanatoryvariables.Toaidin
interpretation,OddsRatio(OR)forassessedriskfactorswerecalculatedbyexponentiationof
thebetacoefficients.TheORrepresentstheratiooftheoddsofanoutcome(BCS4or5)occur-
ringgivenaparticularexposure(elephantdemographicormanagementfactors)comparedto
theoddsoftheoutcomeoccurringgivennon-exposure.Duetolimitedsamplesize,asimilar
analysiswasnotassessedforlowBCS.Furthermore,BCSof1or2wereexcludedfromthis
analysisinordertofocusanalysisonmanagement-basedriskfactorsonhigherBCS,rather
thanlower.StatisticalanalyseswereconductedbyusingSASsoftware,version9.3[PROC
GENMOD,withoptionsREPEATED,CORR=IND,DIST=MULT,LINK=CLOGIT;SAS
Institute,Inc.,Cary,NC].Withtheexceptionoftheunivariatestageofthemodelbuildingpro-
cesswherePvalue<0.15wasconsideredacceptableforcontinuedanalyses,Pvalue<0.05was
consideredstatisticallysignificant.
Results
DevelopmentandTestingoftheAsianBCSIndex
Inter-assessorAgreement. ThepercentagreementforassigningaBCStothesetof40ele-
phantsamongassessorsrangedfrom78%-85%,withthegreatestagreementbetweenassessors
AandC(Table2).WeightedkappavaluesforassessmentsbetweenassessorsAandCwere
interpretedas“almostperfect”agreement,whereasallotherinter-assessoragreementswere
interpretedas“substantial”agreementwhenapplyingthemethodsofLandisandKoch[54].
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Table2. Levelofinter-assessoragreementforassessmentofAsianelephantbodycondition. κ =
w
weightedkappa;95%CI=95%confidenceinterval.
Assessors Avs.B Avs.C Bvs.C
Percentage(%)agreement 83 85 78
κw(95%CI) 0.78(0.63–0.92) 0.82(0.69–0.95) 0.70(0.50–0.88)
doi:10.1371/journal.pone.0155146.t002
BiologicalValidation. TheaveragetriglyceridelevelsfortheBCScategoriesof2–3,4,and
5weresignificantlydifferent(Table3).Therewasnotadifferenceintheaveragetriglyceride
levelsbetweentheBCS2and3categories.TheBCS1categorywasnotincludedintheanalysis
duetosmallsamplesize(N=2).
BodyConditionDistribution
Atotalof240elephantshadcompletestandardizedsetsofphotographssubmittedforbody
conditionassessment.Theseincluded108Asian(n=23males,85females)and132African
(n=26males,106females)elephantsfrom65NorthAmericanzoos.
ThedistributionofBCSforthestudypopulationisshowninFig3withamedianBCSof4
(n=240,range1–5).Collectively,only22%(53/240)oftheelephantshadBCS3.Themajority
Table3. Mean(SD)serumtriglycerideconcentrationsbybodyconditionscore(BCS)category
(N=95).
BCS1 N Serumtriglyceride(mg/dl) SD
1 2 13.0 2.8
2 6 24.0a 14.6
3 14 25.9a 11.2
4 31 34.5b 15.7
5 42 47.7c 21.0
1BCS(1=lowestto5=mostbodyfat)
a,b,cValueswithdifferentlettersaresignificantlydifferent(Pvalue<0.05)
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Fig3.DistributionofBCSofallstudyelephants(n=240,median=4).
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Table4. Bodyconditionscoresforstudyelephantsbyspeciesandsex.
African Asian
Female Male Female Male FullPopulation
N Percent N Percent N Percent N Percent N Percent
106 26 85 23 240
BCS
1 0 0 0 0 2 2.3 0 0 2 0.8
2 0 0 1 3.8 5 5.9 2 8.7 8 3.3
3 23 21.7 10 38.0 14 16.5 6 26.1 53 22.1
4 48 45.3 13 50.0 23 27.1 11 47.8 95 39.6
5 35 33.0 2 7.7 41 48.2 4 17.4 82 34.2
doi:10.1371/journal.pone.0155146.t004
ofelephantshadelevatedBCScomparedtoBCS3,with74%ofelephantsintheBCS4(95/240;
40%)and5(82/240,34%)categories.Only10elephantswererepresentedintheBCS1(n=2)
and2(n=8)categories,collectively,representinglessthan5%ofthestudypopulation(Fig3).
FrequencyofBCSsbyspeciesandsexisshowninTable4.TheprevalenceofBCSabovethe
referenceBCS=3,was74%inAfricanand73%inAsianelephants.Themostprevalent
(mode)BCSobservedinAsianelephantswasa5,whereasthemodeintheAfricanpopulation
wasBCS4.Inmales33%hadaBCSof3,whereas19%offemaleshadaBCSof3.Thecategory
representingthemostbodyfat(i.e.obesity,BCS5)wasobservedin40%offemales,whereas
only12%ofmaleshadaBCSof5.
EpidemiologicalModels
Theresultsofunivariatemodelingofindividualvariablesonbodyconditionscoresarepre-
sentedinTable5.Descriptivestatisticsfortheindependentvariablesincludedinthemulti-var-
iableanalysisareshowninTables6and7.Inthefinalmulti-variablelogisticmodel,the
combinationofWalkWeek,FeedingDiversity,FeedingPredictability,andSexhadthegreatest
effectonriskofanelephanthavingaBCSof4or5comparedtoBCS3(Table8).
UsingtheOddsRatio,eachoftheindividualvariablesinthemulti-variablemodelcanbe
explainedintermsofriskforBCS4or5.WhileOddsRatiosshowtheeffectsofeachvariable
conditionalontheothervariables,itisillustrativetothinkabouttheeffecteachindependent
variablehasontheprobabilityofanoutcomeseparately.WalkWeek7(14ormorehoursof
staff-directedwalkingperweek)wasassociatedwithBCS4comparedtoBCS3andwithBCS5
comparedtoBCS3.Inthemulti-variablemodel,WalkWeek7hadanoddsratioof0.212,
whichcanbeinterpretedasa78.8%decreaseinoddsofelephantsthatexperience14ormore
hoursofstaff-directedwalkingperweekofhavingaBCSabove3ascomparedtoelephants
thatexperienceanyfewerhoursofstaff-directedwalkingperweek.
ThereweretwofeedingvariablesinthefinalmodelincludingFeedingPredictabilityand
FeedingDiversity.TheOddsRatioforFeedingDiversitywas4.692(Table8).Theotherfeeding
variableinthemulti-variablemodel,FeedingPredictability,indicatesthatimplementingan
“unpredictableorrandom”feedingscheduledecreasedtheriskofBCS4or5(Table8).Ele-
phantsthathadanunpredictablefeedingschedulehada69%decreasedriskofBCS4or5as
comparedtoelephantswithapredictablefeedingschedule(Table8).Fig4illustratesthenon-
linearassociationbetweenFeedingDiversityandincreasedriskofBCS4or5forboth“unpre-
dictable”and“predictable”feedingscheduleswhereWalkWeekandAgearekepttothepopu-
lationaverages(2and31.2,respectively).Asthenumberoffeedingmethodsandthe
proportionofthetotalfeedingsessionswhereeachmethodwasusedincreased,therewasan
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Table5. IndependentvariablestestedasriskfactorsforBCS=4or5andstatisticsassociatedwiththeunivariatelogisticregression. OR:Odds
Ratio.
Hypothesis Variable Reference N Beta OR Pvalue
Demographics
+ Age 230 0.040 1.041 <0.001*
0 Sex ref=Male 46
Female 184 1.044 2.841 <0.001*
0 Species ref=African 131
Asian 99 0.579 1.784 0.077^
0 Origin ref=Wild 168
Captive 58 -1.035 0.352 <0.001*
Exercise
- ExerciseWeek ref=1 47
2 85 -0.598 0.549 0.193
4 20 -0.061 0.940 0.933
5 33 -0.566 0.567 0.187
6 5 -1.080 0.339 0.089^
7 15 -1.467 0.230 0.009*
- WalkWeek ref=1 94
2 71 -0.242 0.784 0.562
4 13 -0.540 0.582 0.357
5 12 0.078 1.081 0.902
6 7 -0.869 0.419 0.148^
7 8 -1.486 0.226 0.017*
Feeding
- FeedDay 215 -0.052 0.948 0.290
- FeedNight 215 -0.119 0.887 0.283
- FeedTotal 215 -0.047 0.953 0.223
- FeedingPredictability ref=1 166
2 49 -0.573 0.563 0.125^
- FeedingDiversity 215 1.262 3.533 0.038*
- Spread 215 0.391 1.478 0.647
+ AlternativeFeedingMethods 222 -0.496 0.608 0.465
Housing
+ PercentTimeIndoor 228 -0.010 0.989 0.193
- PercentTimeIn/OutChoice 228 0.002 1.002 0.739
- SpaceExperienceperElephant 228 0.023 1.023 0.002*
- SpaceExperience 228 0.005 1.005 0.009*
Social
- AnimalContact 228 0.037 1.037 0.396
- SocialGroupContact 228 0.031 1.031 0.021*
TrainingandEnrichment
+ RewardingStimuliTechniquesScore Ref=5 11
6 33 1.323 3.755 0.169
7 89 1.710 5.531 0.077^
8 78 1.556 4.743 0.112^
9 2 -21.990 <0.001 <0.001*
- EnrichmentDiversity 213 -0.216 0.805 0.826
^Pvalue<0.15utilizedasthresholdsignificantlevelformodelbuilding
*Pvalue<0.05.BCSs1and2areexcludedfromanalysis.
Hypothesis:+IncreaseoddsofhavingBCS4or5;—DecreaseoddsofhavingBCS4or5;0Neutralrelationship
doi:10.1371/journal.pone.0155146.t005
PLOSONE|DOI:10.1371/journal.pone.0155146 July14,2016 10/20