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RALA-00283;NoofPages199

Research Article

Efficiency of livestock carcass detection dogs

By Inger Hansen and Erlend Winje

On theGround

• There is an increasing use of carcass detection dogsto findremainsofdeadlivestockinNorwe- gianrangelands.Buthoweffectivearethesedogs actually?

• Wecomparedtheefficiencyofapprovedcarcass detection dog equipages (CDEs, i.e., dog and man) withpeoplesearching for sheepcarcasses withoutdogs.

• CDEs found significantly more carcasses than peoplewithoutdogs,andkilometerstraveledand minutesspentpercarcassdetectionindicatedthat dogswere >3xas effectiveintheirsearch.How- ever,CDEsfoundonly1in4ofthecarcasseslaid outexperimentally.

• Thetrainingprogram forCDEsinNorway isnow adjustedtoimprovethequalityoftheequipages.

• The effort of sheep CDEs is important to Nor- wegiansheepfarmersapplyingforcompensation becauseof theincrease inpercentage ofproven lossescausedbyprotectedcarnivores.

• In the future carcass detection dogs in Norway couldbeusedforwildlifeconservationandman- agementtasks.

Keywords: efficiency,cadaver,predation,range- land,sheeplosses,sniffingdogs.

Rangelands43(5):194–199 doi10.1016/j.rala.2021.03.004

© 2021TheAuthor(s).PublishedbyElsevierInc.on behalfofTheSocietyforRangeManagement.This isanopenaccessarticleundertheCCBYlicense (http://creativecommons.org/licenses/by/4.0/)

Introduction

Closeto2millionsheepgrazeonopenrangelandpastures inNorwayeachsummerandaround100,000ofthesearelost asa resultofcarnivores,diseases,andaccidentsevery year.1 In2019,compensationswerepaidfor17,567ewesandlambs thatweredocumentedorassumedkilledbyprotectedcarni- vores (wolverines[Gulogulo],lynx[Lynxlynx],brownbears

[Ursusarctos],gray wolves [Canis lupus],and goldeneagles [Aquilachrysaetos]).2AlthoughinspectionsofsheepinNor- wegianmountainandforestrangesarefrequent,3 itischal- lengingtofindsheepcarcasseswithinlargegrazingareasand carcassescanbehiddeninvegetationoraninaccessibleloca- tion.Furthermore,carnivores,scavengers,and maggots(i.e., flylarvaefoundindecayingmatter)consumepartsofthecar- cassleavingonlydrybonestobefound.Infact,lambcarcasses canbegonewithin24hoursafterdying.4Toreceivecompen- sationsforsheepkilledbylargecarnivores,farmersneedtolo- catecarcassesandtheNorwegianNatureInspectorate(NNI) hastoprovethatprotectedcarnivoresmostlikelyarethecause ofdeath,orthereareothercircumstancesshowingpredom- inanceofprobabilitiesthatthesheeparekilledbylargecar- nivores.5However,<10%oflivestocklossescompensatedare provenbytheNNIasdepredated.6

Dogs’sense of smell is far better than that of humans.

Humans have about5 million olfactory receptors,whereas dogs(bloodhounds)have>100million.7 Dogscansmellan item with particle concentration levels at one to two parts per trillion.8 Thus,dogs have been used for olfactory dis- crimination (nonbiologicalscents and biologicalscents)for decades,suchasdetectionofbombs,drugs,cancer,andhuman remains.9-12 Owing to their extensive olfactorycapabilities, dogsareincreasinglybeingusedinwildlifemanagementand conservationinarangeoftasksincluding1)locatingwildlife andassessingpopulationstatus,2)facilitatingspecimenand carcasscollection,3)detecting scat,4) capturingandmark- ing wildlife,5) studyingwildlifebehavior,and6) managing wildlifedamage.13

Dogs searchingfor birdand batcarcassesatwindfarms had a higherdetection ratethan humans (80% vs.20%).14 In anotherstudy,songbirdcarcasseswererecoveredapprox- imately12:1tothosemissedfordogsand1:1forhumans.15 However,onlyrecentlyhavedogsbeentrainedtolocatethe remainsoflivestockcarcasses.Whichodorsareusedbydogs intheirsearchforcarcassesarenotknown,butsometypical volatileodorsfromcadaversarecadaverineandputrescin.16

NorwegianCarcassDetectionDogs17(NCDD)isanor- ganization aimed at improving the competence of carcass detectionequipages (CDEs,i.e.speciallytrained dogs with guides).Withexperiencefrompreparationofrescueandmil- itarydogs,theassociationhasdevelopedacourseandanap- proval testfor CDEs.The basic courseconsists of3 hours oftheoryand 4hours ofindividualtraining.Tobecomean approvedequipage,onemustcompletethebasiccourse,find

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3outof4carcassesorobjectsplacedinalimitedforestarea (approvaltest),anddocument≥30hoursofactivesearching for sheepcarcassesinopen rangelands.Asof August2019, 207 equipages havebeen approved.Thetraining ofdogs is basic with alow threshold,meaningthat classic condition- ing/positive reinforcementisusedto encouragethe dogsto find carcasses.18-20 Positivereinforcement strengthensa be- havior byrewardingthedog.Indeed,foracanine,findinga carcassisapositivereinforcementinitself.Furthermore,itis possible for“ordinary” dogowners tojointhecourse.Thus, thelevelisadjustedtosheepfarmers(andothers)whowould liketoincreasethesuccessofsheepcarcassdiscoveriesintheir own(andothers)grazingareas.

OurstudydocumentedtheefficiencyofCDEsinfinding deadsheep.Ourresearchquestionswere1)howmuchbetter areCDEscomparedwithhumanswithoutdogsindetecting sheepcarcasses,and2)areCDEsasgoodatfindingfreshand hiddencarcassesasoldandopensitedones?

Materialandmethods

Dogsandfieldstaff

Atotalof16trainedCDEsthathadpassedtheNCDD approvaltestand16trainedpersons(sheepfarmersorshep- herds)withoutdogsparticipated.NCDDhelpedusinselect- ing CDEswithinthe geographicalregionsofeachtestsite, andtheregionalagriculturalofficeassistedusinfindingexpe- riencedsheephandlers.Windspeed(calm,moderate,windy) andprecipitation(none,moderate,heavy)werenoted.Allthe CDEscarriedouttheirsearchesinheadwinds,asfaraspossi- ble,andalldogswereona20-mlongleashduetotheprotec- tionofwildanimalsandgrazing livestockduring1Aprilto 20August.21TracksandcarcasspositionswereGPS-logged.

Experimentaltrials

Intensivesearcheswereconductedin10fieldsof0.5km2 (123.6 acres) each,at first with a dog (n=10 CDEs) and thenbyapersonwithoutdog(n=10).Withineachfield,8 lambcarcassesweighing2to4kgwereputoutinan2×2 factorialdesign; 2 carcasseswere “fresh” (frozenwhenday- fresh,thawed,andplacedintestfieldthesameday)and“hid- den” (undervegetation,stones,etc.);2werefreshandlocated

“open” (laidrightattheground);2were“old” (frozenwhen day-fresh,thawedandlaidoutintestfieldafter3-4days)and hidden;and2wereoldandplacedintheopen.Atotalof4 hours searching timewas given(8 hours per km2 [8hours per247.1acres]).Allexperimentalfieldswerelocatedwithin scatteredmountainforestareas.

Fieldtrials

Partsof6outfieldpasturesforsheep,sized4km2(988.4 acres) each, were investigated for dead sheep by CDEs (n=6)andpersonswithoutadog(n=6)simultaneously.The

searchingtimewassetto32hours(intensivesearch;8hours perkm2),butinorderforthepairofpersonnelwithandwith- outadogworkinginthesamefieldnottoseeeachother,9 days separatedthem.Theaverageratesoflambslost inthe grazingareasselectedhadtobe≥10%overthelast3years.All typesofcarcassdiscoverieswererecorded,rangingfromwhole carcassestosmallboneremnantsandpiecesofwool/fur,re- gardlessofanimalspecies(Fig.1).Anycarcassremainswithin a20-meterradiuswasconsideredasonecarcassfinding.Staff fromtheNNItrainedfordocumentingwhetherlivestockare killedbyprotectedcarnivoresornotwereusedtodiscriminate predationfromothercausesofmortality.

Statistics

Allmeasureswerestandardizedto8hourssearchperkm2 (i.e.,amount of effort).In orderto measure the search ef- ficiency,themeannumberof kilometersand minutesspent per carcass detectionwere calculated. Number of carcasses foundwithandwithoutdogs,bothintheexperimentaltrials andinthefieldtrialsdidnotfollowthenormaldistribution (Kolmogorov-SmirnovTest).Thus,pairwisedifferenceswith andwithoutdogsregardingthetotalnumberofcarcassde- tectionsandnumberoffindsbycarcasstype(freshandopen;

freshandhidden;oldandopen;oldandhidden)weretested using Wilcoxon SignedRank Test.Chi-squared goodness- of-fit testswereusedto testifthe typesof carcassesfound bydogsintheexperimentaltrialswererandomlydistributed.

Differences indistance(kilometer)searchedwithandwith- outdogsinbothtypeoftrials,andkilometersandminutes per carcassfindinthefield trialswerenormally distributed andtestedwithpairedt-tests.Thesignificancelevelwassetto 0.05.Datawasprocessedwiththestatisticssoftwarepackage Minitab17.22

Results

Experimentaltrials

TheCDEsfound 19outof80lambcarcasses(detection rate23.8%),whereaspersonswithoutdogsonlyfound2(de- tection rate2.5%;confidence intervalsdo notoverlap,P<

0.05,Fig.2).Fivecarcassesdetectedbythedogswerefresh andlocatedintheopen,fourwerefreshandhidden,whereas fivewereoldandintheopenandfivewereoldandhidden (χ2=0.158,P >0.5).Thus,the dogsfound carcassesthat wereassumedthemostdifficulttodetect(freshandhidden) just asoftenastheonesthatwereassumedeasier.Thetwo carcassesfoundbypeoplewereoldandlocatedinopensite.

Themeandistancessearchedperfieldwithandwithoutdogs wereindifferent(9.6vs.9.7km,T=–0.1,P>0.5).Thedogs showed individualvariationindetectionrate,rangingfrom twodogsfindingnocarcasses(trialsFandG,Fig.2)totwo dogsthatfound50%ofthecarcasses(trialsAandH,Fig.2).

In general,the track logsshowed extensive andsystem- aticsearches,bothwithandwithoutdogs.However,searchers

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Figure1. Acarcassdetectiondogduringafieldtrialthathasfoundanoldbonefromasheep.TheGPSposition(universaltransversemercator projection(UTM)coordinates)ofthecarcassislogged.

0 2 4 6 8 10 12 14

0 1 2 3 4 5 6 7 8

Trial A Trial B Trial C Trial D Trial E Trial F Trial G Trial H Trial I Trial J

Distance (kilometer) searched

dnuof sessacrac fo rebmuN

Carcasses with dog Carcasses without dog Distance with dog Distance without dog

Figure2. Numberofcarcassesfound,anddistance(kilometers)searchedperfieldwithandwithoutdogsinthe10experimentaltrials.

withoutadog,butalsosomeoftheCDEs,passedseveralof thecarcassesclose(<10meters)withoutfindingthem.

Fieldtrials

In the six rangeland pastures,CDEsdetected a total of 132carcassremains,whereassearcherswithoutdogsfound76

(Table1).Twoofthedogfindswerehidden(buried)and25 werefromthepresentgrazingseason.Allcarcassesfoundby peoplelaidonopengroundand13werefromthepresentyear.

Onlythreecarcasseswerefoundinaconditioninwhichthe causeofdeathcouldbedocumented(i.e.,freshandenough leftofthebody).Twoofthesewerelocatedbypeoplewithout dogs(onedocumentedbyNNIbeingkilledbywolverineand

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Table1

Numberofcarcassesfound,distancesearchedperfieldtrial(kilometer),andkilometersandminutesspentpercarcassdetected(mean±SEM),andrange (minimum-maximum),withandwithoutdogsinthe6fieldtrials

Withandwithoutdogs Mean±SEM Range(min-max) Differencewithand

withoutdogs

Numberofcarcassesfound Withadog 21.7±7.6 4.0-58.0 CIsoverlap

P>0.5

Withoutadog 12.7±5.3 0.0-30.0

Kilometerssearchedperfield Withadog 63.4±6.8 41.0-83.7 T=–1.34

P>0.05

Withoutadog 75.9±4.1 63.3-88.8

Kilometerstraveledper carcassdetected

Withadog 5.8±2.7 0.8-18.6 T=–1.31

P>0.05

Withoutadog 20.4±14.4 2.8-77.5

Minutespercarcassdetected Withadog 161±65.6 33.1-480.0 T=–1.27

P>0.05

Withoutadog 516±356 64.0-1920.0

Confidenceinterval(CI)indicates;SEM,standarderrorofmeans.

onediedinanaccident),andthethird(documentedbyNNI aspossiblykilledbywolverine)wasfoundbya CDE.More than 95% of the finds conductedboth bydogs and people consistedofsmallbonefragmentsand/orwool.

Bycombiningthedetectionrates(d.r.)intheexperimen- taltrialsforCDEs(23.8%)andpeople(2.5%),weestimated thetotalnumberofcarcassesinthefieldstobebetween555 (based onthe CDEs’d.r.)and3,040(basedon thepeoples’

d.r.).The“best”CDEinthefieldtrialsdetected13timesmore carcassesthanthepersonwithoutadog(13vs.1),whereasthe

“least” effective CDEdetected 1.4times lesscarcassesthan thesearcheralone(19vs.26).TheotherCDEsfound1.2to 4.2timesmorecarcassesthanpersonswithoutdogs.

Duetothevariationinnumberofcarcassesfoundinthe fieldtrialsandalimitednumberoffields(Table1),nosignif- icantdifferenceswithorwithoutdogswerefoundregarding numberofcarcassesdetected,distancesearchedorkilometers, andminutesspentpercarcassfound.Nevertheless,themean numeric valuesofkilometersandminutesspent percarcass findwere>3xofthatforpeoplewithoutdogs,indicatingthat CDEsweremoreefficientthanpeoplealone(Table1).

Discussion

TheexperimentaltrialsshowedthatCDEswere9.5times better thanpeople aloneatfinding sheepcarcasses(success rate:23.8%vs.2.5%),andthefieldtrialsindicatedthatCDEs were>3times aseffectiveintheirsearch,measuredinkilo- meters,andminutespercarcassdetection.Furthermore,the dogsfoundalltypesofcarcassesjustaseasily.Thedogswere superior to people in finding hidden carcasses.Our results areinaccordancewithotherstudiescomparingdogsandhu- mansforcarcassdetection,suchasfindingpasserinecarcasses in densevegetation15 andbird and batcarcass detectionat windfarms.14delValleetal.14foundthathumansperformed poorlyatdetectingsmallcarcasses(∼20%detectionrate)and moresoindensevegetation.Wedidnotmeasurethesizesof thecarcasses,butpredominantlythecarcassesdetectedinthe fieldtrialsconsistedofsmallboneremainsand/orwool.

Resultsfromtheexperimentaltrials,however,documented thatthe CDEsdidnotfindmorethaneveryfourthcarcass outinthefields.AsdiscussedinthereviewarticlebyTroisi etal.,23andbasedonexperiencesfromourstudy,webelieve thatwinddirection,overlywidesearchloops,distractionsby otherscents,ormisinterpretedorabsenceofcommunication betweendogandhandlermayexplainsomeofthefailureof CDEstodetectcarcasses.Furthermore,weexperiencedthat some dogs being “on duty” several days in advance of the testfailed.NCDDbelievesaday-longintensivesearchistoo muchfor adog tomaintain fullmotivationand concentra- tion.Thedoghandlershouldknowhowtomotivatethedog andapplythistotraining andworkingsituations.Therela- tionship betweenthehandlerand thedog issignificant for workingdogs.23,24 Likewise,hottemperatureswillaffectthe activity levelofdogs andtheir sniffingefficiencynegatively becausedogscannotpantandsniff atthesametime.Inone ofthefieldtrialsthetemperatureincreasedabove30°C(85°F) on8August,andthedoghandlernotedthedogwas“lazy” all day.

Olfactory abilities vary both within and between dog breeds,accordingtothesizeofthecanineolfactorybulband thegenesthatcontroltheolfactoryreception.10,12,25Indeed, intheexperimentaltrialswedocumentedvariationindetec- tionratebetweenthetwodogsthatdidnotfindanycarcasses (trials F and G,Fig.2)to the two dogsthat found halfof the carcasses(trials AandH,Fig.2).In thefield trials,the numberofcarcassesdetectedwithdogscomparedwithfinds madebypersonsalone(withineachfield)variedevenmore, from13to0.7.However,thesetestfieldsdifferedinthenum- berofcarcassespresentandthetotalnumberofcarcasseswas notknown,thusitwasnotpossibletocomparethedetection ratesbetweendogs.

ItisimportantthatCDEsmaintainahighdetectionrate, especiallyiftheworkispaidfor.Byusingdogsthatarefos- tered and trained by their owners it is possible to educate CDEs at a large scale with limited resources.26 How high the competencelevel shouldbeis atrade-off betweenhav- ingmany"mediumquality"CDEsavailableandafewexcel- lentones.NCDDwasnotsatisfiedwiththeresultsfromthe

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experimental trials. To increase the CDEs’ success rate, NCDDhasnowimprovedtheirtrainingprogrambyoffering acomprehensivecourseandbyprovidingapprovedequipages withadditionaltrainingsessions.

Thefactthatfew freshcarcasses,inwhichwewereable to document the cause of death were found,confirms that itisdifficult tobeintherightplace attherighttime.This hasalsobeenconfirmedinothertrials.27Inanacutesituation withcarnivoreattacks(i.e.,massivedepredationoflivestock, limitedintime andspace),theconditionsaredifferent;the CDEswill besearchingfor acluster offresh killswithina smallpartofthegrazingarea,helpingtoidentifytheextent ofthe damage.Whereassearching forcarcassesthroughout an entire rangeland pasture(most of them sized >50km2 [2,355 acres]),is likesearching for a needle ina haystack.

Thus,thisprojecthasstrengthenedouropinionthatbestre- sults areachieved byCDEs whenused in acute situations.

Despitethis,dogsareabettertool thanpeople alonehelp- ing farmers tofind dead animals,otherwise every livestock animalwillneedtohaveaGPS-transmitterwithamortality function.

Conclusionsandimplications

CDEsweremoreeffectiveatfindingsheepcarcassesthan searcherswithoutdogs,measuredintotalnumberofcarcasses discoveredaswellaskilometersand minutesspentpercar- cassfind.Thedogsfoundalltypesofcarcassesjustaseasily andwereparticularlybetterthanpeoplealoneinfindinghid- dencarcasses.However,theexperimentaltrialsshowedthat CDEsdetectedonlyoneinfourofthecarcasseslaidout.Our results have led to revisions of NCDD’s training program.

NCDDisnowofferingacomprehensivecourseandtheyare following-uponapprovedCDEsmoreclosely.Itisimportant forCDEstotrainoncarcassesthatarelaidoutinthefieldall yearround.Basedonexperiencesfromthisprojectaguidefor CDEswasoutlined.28

TheeffortofcarcassdetectiondogsisimportanttoNor- wegiansheepfarmersapplyingforcompensationstoincrease thepercentageofprovenlosses.In thefuturecarcassdetec- tiondogsinNorwaymight alsobeusedtodocument dead and injuredbirdsatwind farms(specially protected species likegoldeneagle,seaeagle[Haliaeetusalbicilla]andEurasian eagle-owl[Bubobubo]),orforotherwildlifeconservationand managementtasks.13

DeclarationofCompetingInterest

Theauthorsdeclarethattheyhavenoknowncompeting financial interestsor personalrelationships that couldhave appearedtoinfluencetheworkreportedinthispaper.

Acknowledgments

WewouldliketothankNilsSteinvikandJohnnyMath- ieseninNorwegianCarcassDetectionDogsfor facilitating thefieldexperiments,aswellasthefieldstaff withandwith- outdogsparticipatinginthetrials.ThankstoGreteMeisfjord JørgensenandJoJoremAarsethforperusalofthetext.

This work was supported by mitigating- and conflict- reducing grantsfromTheCountyGovernors ofFinnmark, Troms,Nordland,Sør-Trøndelag,MøreogRomsdalandOp- pland.

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