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SupportedbyBotic´arioGroupFoundationforNatureProtection

https://www.journals.elsevier.com/perspectives-in-ecology-and-conservation/

Research

Letter

Assessing

the

consistency

of

hotspot

and

hot-moment

patterns

of

wildlife

road

mortality

over

time

Rodrigo

Augusto

Lima

Santos

a,b,c,d,∗,1

,

Fernando

Ascensão

e,f,1

,

Marina

Lopes

Ribeiro

c

,

Alex

Bager

g

,

Margarida

Santos-Reis

d

,

Ludmilla

M.S.

Aguiar

a,b

aCursodePós-Graduac¸ãoemEcologia,InstitutodeCiênciasBiológicas,UniversidadedeBrasília,Brasília,DF,Brazil bLaboratóriodeBiologiaeConservac¸ãodeMorcegos,DepartamentodeZoologia,UniversidadedeBrasília,Brasília,DF,Brazil cInstitutoBrasíliaAmbiental(IBRAM),Brasília,DF,Brazil

dCentreforEcology,EvolutionandEnvironmentalChanges(Ce3C),FaculdadedeCiências,UniversidadedeLisboa,Lisboa,Portugal eCentrodeInvestigac¸ãoemBiodiversidadeeRecursosGenéticos(CIBIO/InBio),UniversidadedoPorto,Vairão,Portugal

fCentrodeEcologiaAplicada“ProfessorBaetaNeves”(CEABN/InBio),InstitutoSuperiordeAgronomia,UniversidadedeLisboa,Lisboa,Portugal gDepartamentodeBiologia,UniversidadeFederaldeLavras,Lavras,MG,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received10August2016 Accepted6March2017 Availableonline27March2017 Keywords: Roadsegments Roadkill Aggregations Scaleeffect Mitigations

a

b

s

t

r

a

c

t

Spatialandtemporalaggregationpatternsofwildlife-vehiclecollisionsarerecurrentlyusedtoinform whereandwhenmitigationmeasuresaremostneeded.Theaimofthisstudyistoassessifsuch aggre-gationpatternsremaininthesamelocationsandperiodsovertimeandatdifferentspatialandtemporal scales.Weconductedbiweeklysurveys(n=484)on114kmofnineroads,searchingforroadcasualties (n=4422).Aggregationsweresearchedusingdifferentlengthsofroadsections(500,1000,2000m)and timeperiods(fortnightly,monthly,bimonthly).Ourresultsshowedthathotspotsandhot-momentsare generallymoreconsistentatlargertemporalandspatialscales.Wethereforesuggestusinglongerroad sectionsandlongertimeperiodstoimplementmitigationmeasuresinordertominimizethe uncer-tainty.Wesupportthisfindingbyshowingthattheproportionalcostsandbenefitstomitigateroadkill aggregationsaresimilarwhenusingdifferentspatialandtemporalunits.

©2017Associac¸˜aoBrasileiradeCiˆenciaEcol ´ogicaeConservac¸˜ao.PublishedbyElsevierEditoraLtda. ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(

http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Roadshavea varietyofecologicaleffects ontheir surround-ingenvironment,andoneofthemoststudiediswildlife-vehicle collisions(WVC)(Formanetal.,2003; Reeetal.,2015).Several researchershave demonstratedthatroadkillsareoftenspatially andtemporallyaggregated,hereafterreferredasWildlife-Vehicle Aggregations(WVA).WVA aregenerallyrelated tospecies’ bio-logicaltraits(e.g.mating),roadfeatures(e.g.trafficvolume),the surroundinglandscapeorclimateconditions(Gunsonetal.,2011; Maloetal.,2004;Smith-PattenandPatten,2008).Therefore,WVA mayindicatepreferentialtargets(hotspotsandhot-moments)for implementing mitigation measures (Malo et al., 2004; Morelle etal.,2013;Reeetal.,2015).TheidentificationofWVAisoneof

∗ Correspondingauthor.

E-mailaddress:rodrigosaantos@gmail.com(R.A.LimaSantos). 1Theseauthorssharethefirstauthorship.

theapproachesmostusedbyresearchersanddecisionmakersto implementmortalitymitigationonroads(Santosetal.,2015).

Mitigationmeasuresmustbeplannedtoensureeffectiveness, duetothehighcostofinstallationandmaintenance(Reeetal., 2015).Thus,itisnecessarytodeterminethebestspatialscale(s)at whichputativepredictorsindicatelocationsofWVA(Langenetal., 2007;Reeetal.,2015).Ideally,WVAneedtobespatiallyrestricted inlength,sinceshortroadsectionscanbemoreeasilymitigated byfaunalpassagesanddriftfencingthanwhenWVAsegmentson roadaredistributedoverabroaderextentoftheroad(Langenetal., 2007).Ontheotherhand,understandingtheroleofseasonalityon roadmortalityallowstheidentificationofpossibleWVAincertain periods(hot-moments),anddecisionmakerscandirectmitigation measurestowardtheperiodofhigherWVA,whichwillreducethe costs(Sullivanetal.,2004).

The aim of this study was to investigate if the spatial and temporal patterns of WVA were similar during the same time periodforthedifferenttaxonomicgroups. IfWVAoccur consis-tentlyin thesamelocation andtime period, i.e.do notchange overtime,mitigationmeasuresappliedthereinwillprobablybe http://dx.doi.org/10.1016/j.pecon.2017.03.003

1679-0073/©2017Associac¸˜aoBrasileiradeCiˆenciaEcol ´ogicaeConservac¸˜ao.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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more cost-effective(Costa etal., 2015).Additionally,we evalu-atedhowdifferentroadsegmentlengthortimeperiodaffected theconsistencyofspatialandtemporalWVA patterns.We con-siderthathighercorrelationofWVApatternsbetweenconsecutive years indicatehigherreliability inusing suchlocationsas miti-gationtargets.Hence,weevaluatehowcost-benefiteffectiveness couldvarywhentargetingmitigationtoshort/longroadsectionsor timeperiods.Cost-benefitanalysiscanbecomplexinroadecology (Costaetal.,2015).Here,weadoptasimpleapproachwherewe countthenumber ofcasualtiesthatcouldhavebeenprevented

if road mitigation was implemented in WVA (assuming full effectiveness).

Materialsandmethods

Studyarea

WeconductedthestudyinBrasília(FederalDistrict),locatedin theCerradobiomeofCentralBrazil.Atotalof114kmpertaining toninedifferentroadsweresurveyed.Moredetailsofthestudy

500 m

A

B

5 4 3 2 1 5 4 3 2 1 5 4 3 2 1 5 4 3 2 1 5 4 3 2 1 5 4 3 2 1 5 5 4 4 3 3 2 2 1 1 AprilMayJune July August

SeptemberOctoberNovemberDecemberJanuaryFebruary

March AprilMayJuneJulyAugust

SeptemberOctoberNovemberDecemberJanuaryFebruary

Mar h April June

August October DecemberFebruary

0 50 100 150 200

Fortnightly Monthly Bimonthly

Amphibians Reptiles Birds Mammals 0 30 60 Road section Time period Year Year 90 0 20 40 1000 m 2000 m Amphibians Reptiles Birds Mammals

Fig.1.Locationofwildlife-vehicleaggregations(WVA)peryearandclass,alongthe114kmofroadsurveyed(A)andalongtheyear(B).Eachverticalpanelpresentsthe locationswhenusingdifferentspatial(A)ortime(B)unitstodetectWVA.

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area,includingweatherconditions,traffic,roads,protectedareas monitoredandamapareprovidedinText1inAppendix1. Datacollection

Weconductedroadsurveysbiweekly(twosurveys/week)for5 years,surveyingall114kmbycampaign(i.e.,allroadtypeswere surveyed equally), between April 2010 and March 2015, total-ing480roadkillsurveys.Twoobserversandonedriversearched forroadkillsin avehicletravelingatca.50km/h. Theobservers recorded thelocation of carcasses using a hand-held GPS (5m accuracy).Carcasseswereremovedafterdatacollectiontoavoid pseudo-replication and recounting carcasses. Domestic animals werenotconsideredinfurtheranalyses.

Dataanalyses

WVCrecordswereaggregatedbyclass(amphibians,reptiles, birds,andmammals)andyear,andseparatedatasetsforthe spa-tialandtemporalinformationwerecreated.Forthespatialdataset, weaggregated therecords byroad segmentsof500, 1000 and 2000mlength.Thetemporal datasetwasaggregatedusing fort-nightly,monthlyandbimonthlytimeperiods.Weconsideredayear ofsurveyasthetimebetweenAprilandMarchofthefollowingyear. Hereafterwewillrefertothesectionlengthsandtimeperiods asunits.

Foreachclassandyearofsurveyweassumedthattheobserved numberofroadkillsperunitwouldfollowarandomPoisson dis-tributionwithamean()equaltothetotalnumberofroadkills dividedbythetotalnumberofunits.Theprobabilityofanyunit havingxnumberofcollisionswastherefore:

p(x)= x x!e

Ameanvalue()foreachtaxawascalculated,andconsidering roadkillsperyear.Asthemean()variedacrosstaxa,each500mof roadsectionwiththreeormorecollisions,couldbedefinedasWVA forAmphibians.Roadsectionswithfourormorecollisionswere classifiedasWVAforReptiles,tobirdssevenormorecollisions,and formammalswiththreeormore.TheseminimumvaluesforWVA detectionincreasedforlongerroadsections(1000mand2000m) scales.Forhot-moments,periods(fortnight)withfiveormore colli-sionscouldbedefinedasWVAforAmphibians.ForReptiles,periods (fortnight)withthirteenormoreroadkillswereclassifiedasWVA, andtobirdsthirtythreeormoreroadkills.Theseminimumvalues forWVAdetectionincreasedforlongertimeunits(monthlyand bimonthlytimeperiods).

WeconsideredaunittobeaWVAwhenp(x)>0.95.Weusedthe falsediscoveryratetoreducethelikelihoodofdetectingfalseWVA (TypeIerror)duetomultipletesting (Benjaminiand Hochberg, 1995). We usedthesame approach of Maloet al., (2004)as it permitseasycomparisonamongsamplingschedulesusingafixed spatialscale.Besides,thismethodseemstoperformbetterthan otherstodetectfatalityhotspots (Gomes etal.,2009).We then transformedtheconsecutiveunitsintoabinaryvariableof pres-ence/absenceofWVA.Hence,foreachyearthereisahot-moment andahotspotevaluationforeachtaxonomicclass.

ThesimilarityofWVApatternsovertimewasassessedusing correlationtestsbetweenconsecutiveyearsusingthePhi coeffi-cient(rPhi)(Zar,1999).ThePhicoefficientmeasuresthedegreeof

associationbetweentwobinaryvariables,anditsinterpretation issimilartothecommoncorrelationcoefficients.Thisprocesswas performedforeachaggregationunit(spatialandtemporal).Finally, thecost-benefitanalysiswasperformedforeachtaxa, yearand unit,byrelatingtheproportionofroadsectionsortimeperiods that were classified as WVA with the proportion of casualties

potentiallyavoidedifthoseWVAweremitigated.Allcalculations andplotswereperformedusingRsoftware(RCoreTeam,2015) andtheRpackagesHmisc,vcd,cowplotandggplot.

Results

Werecorded4422non-domesticroad-killedanimals,ofwhich 5%wereamphibians(n=274,9species),15%reptiles(n=690,34 species),71%birds(n=3009,91species),and9%mammals(n=448, 24species)(TablesS1andS2inAppendix1).Wedetectedseveral WVAinallclassesforallspatialandtemporalunitsconsidered, exceptformammalshot-moments(Fig.1AandB).

1.00

A

B

0.75 0.50 0.25 0.00 1.00 0.75 0.50 0.25 0.00 Birds Phi coefficient Phi coefficient 500 m 1000 m 2000 m Mammals Reptiles Amphibians Birds Reptiles Amphibians

Fortnightly Monthly Biomonthly

Fig.2.Phicorrelationsbetweenconsecutiveyears,perclassandaccordingtothe spatial(A)ortemporal(B)unitusedtodetectWVA.

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500 m

A

B

0.6 0.75 0.50 0.25 0.00 0.75 0.50 0.25 0.00 0.75 0.50 0.25 0.00 0.75 0.50 0.25 0.00 0.0 0.1 0.2 0.3 0.4 0.5 0.4 0.2 0.0 0.6 0.4 0.2 0.0 0.6 0.4 0.2 0.0 0.6 0.4 0.2 0.0 0.0 0.1

Proportion of road with mitigation Proportion of road with mitigation

Propor

tion of casualties potentially a

v

oided

Propor

tion of casualties potentially a

v oided 0.2 1000 m 2000 m Amphibians Amphibians Reptiles Reptiles Birds Birds Mammals Mammals

Fortnightly Monthly Biomonthly

Fig.3.Cost-benefitassessmentusingtherelationbetweentheproportionofcasualtiesthatcouldpotentiallybeavoidedwiththeproportionofroad(A)oryear(B)that wouldbemitigated.Linesrepresentthegainintheproportionofcasualtiesrelativelytoincreaseinmitigation.Thestraightlinerepresentsthe1:1gain,i.e.whenincreasing themitigationin1%onewouldexpectanincreaseinavoidedcasualtiesof1%;thefollowinglinesrepresent,respectively,thegains1:2,1:3,1:4and1:5.

Regardingthespatialdataset,whenusingunitsof500mand 1000m,mostWVAwereidentifiedonlyonceineachclass(Fig.1A). However,this patternwasnotconsistentacrosstheclasses.For example,when usinga unitof 1000m, we detectedonly 4%of sectionsthat wereWVA foramphibiansinmorethanoneyear, whileforbirdsthisproportionascendedto14%.Nevertheless,we foundoveralllow correlationvalues (rPhi<0.5)between

consec-utiveyearsinWVApatternsforallclassesforthesesmallerunit lengths(Fig.2A).Conversely,when usingthelongerunitlength (2000m)thenumberofsectionsthatwereclassifiedasWVAmore thanonceincreased,e.g.9%foramphibiansand23%forbirds. Like-wise,thesimilarityinWVApatternswashigher,particularlyfor amphibiansandreptiles,withvaluesofrPhiwellabove0.5(Fig.2A

andFigureS1inAppendix1).Surprisingly,thesameWVAsections thatoccurred(km10and38forroadsplitin2000m,Fig.2A)for alltaxawerelocatedinfour-laneroads(FigureS2inAppendix1). Thecost-benefitevaluationsuggestsasimilarpatternacrossunit length,withineachclass.Forexample,5–10%mitigationoftheroad couldpotentiallyresultinanavoidanceof20–50%ofcasualtiesfor amphibians,reptilesormammals.Infact,fortheseclasses,when

usingaunitlengthof2000m,therelationoftheproportionof casu-altiespotentiallyavoided(benefit)wasgenerally4foldgreaterthan theproportionofroadmitigated(cost);whileforbirdsthebenefit was2foldgreater(Fig.3A).Hence,planningmitigationusinglarger roadsectionsisapparentlymoreeffectiveasitincorporatesmore WVAfromdifferentyears,andyetdoesnotrepresentadecreasein thecost-benefitrelation.

Regarding the temporal dataset, we found higher similarity inWVApatternsinconsecutiveyearswhenusingthethree dif-ferent timeunits,exceptformammals,which wasmore evenly distributedthroughouttheyear(Fig.1B).Highercorrelationswere detectedwhenusinglongertimeunits(bimonthly),particularlyfor amphibiansandbirds(medianrPhi>0.75)(Fig.2B).Theperiodsof

highestroadkillforamphibianswerebetweenOctoberand Novem-ber;forreptilesbetweenFebruaryandMay(andpeaksatDecember and January);andfor birdsbetweenOctober andMarch.These aggregationperiodswereconsistentlyhighlightedinthedifferent units(Fig.2BandFigureS3inAppendix1).Ingeneral,usinglonger timeunitstodetectWVAwerealsoaseffectiveasshorterunits. Forexample,applyingmitigationforabouttwoandhalfmonths

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(20%ofyear) wouldpotentiallyavoidca. 50–75%ofroadkillsof amphibians.Forreptiles,theidentificationofWVAusinglonger timeunit(bimonthly)highlighted2–6monthsofhighermortality, whichisprobablyrelatedtothediversityofspeciesincludedinthis classthathavedifferentpeaksofmovementandtherefore mortal-itythroughouttheyear(e.g.turtlesandlizards).Inallcases,the relationbetweentheproportionofcasualtiespotentiallyavoided wastwofold(ormore)theproportionof yearundermitigation (Fig.3B).Therefore,theuseoflongertime-periodsispreferable asitpotentiallyincludesWVAsfromdifferentyearsandagaindoes notrepresentadecreaseinthecost-benefitrelation.

Discussion

Inthisstudyweaimedtoassesstheconsistencyof hotspots andhot-momentsovertime,i.e.,wequestionedifasignificant pro-portionofWVAoccurinthesamesites/periods,andifthepattern wasmaintainedatdifferentspatialandtemporalscales.Ourresults showedthatWVApatternsaremoreconsistentwhenusinglarger spatialandtemporalunits.Moreover,althoughintuitivelyonemay thinkthatmitigationplansshouldtargetwelldefinedandshort roadsectionsortimeperiodstoincreasethecost-benefitresources, weshowthattheproportionalcostsandbenefitsaresimilar regard-lessofthespatialandtemporalunitsusedtodetectWVA.Although moreresourcesarerequiredwhenmitigatinglongersectionsor timeperiods,thenumberofcollisionspotentiallyavoidedisalso higher.Thesepatternsarewellillustratedbythenumeroussections classifiedasWVAwhenusingsmallerspatialortimeunits,many ofwhicharenotconsistentacrosstheyears.Hence,largerunits mayguaranteemorereliableinformationonwhereandwhento allocatemitigationmeasures.Importantly,withineachWVA, mit-igationshouldfocusonbroad-scaleoftheroadsectionorperiod asroadkillsmayoccuratdifferentpointsormomentsindifferent years.

Mitigationmeasuresfocusedonsinglepointlocations(e.g., cul-verts)isunlikelytobesufficienttomaintainthelong-termviability ofpopulations(Patricketal.,2012).We suggestthatmitigation shouldfocusbroad-scalemeasuresdeployedatlongerroad sec-tionsandtimeperiods,althoughthesearemoreexpensivetobuild andmaintain(Beaudryetal.,2008;Patricketal.,2012).Few meas-urescanbeimplementedat largescales,suchas thereduction ofspeed limits(Hobday and Minstrell,2008), velocityreducers anddriftfencesconnectingtofaunalunderpasses(Ascensãoetal., 2013;Reeetal.,2015).Differentstrategiescanbeadopted,which willdependon thefinancial resourcesavailable and thetarget species.Forinstance,manysmallcrossingsundergroundcanbe implementedifturtlesarethetargetspecie(Beaudryetal.,2008). Also,ourresultshighlightedthefour-lanesectionsaspriority sec-tionstomitigate,suggestingthatthe“true”WVAisareflectance ofhightraffic,sincetheseroadssegmentsshowsthehighesttraffic volumesinourstudyarea.

ThetemporalanalyzesrevealedastrongassociationofWVAof amphibians,reptilesandbirdswiththerainyseason(Octoberto Marchinourstudyarea).Thisperiodcorrespondstotheoccurrence ofmigratoryeventsand/orbreedingseasonformanyspecieshere recorded(Sick,2001;Coelhoetal.,2012).Previousworkshavealso reportedincreasedmortalityratesduringwarmandwetseasons, whiledryorcoldseasonsgenerallypresentlowervalues(Coelho etal.,2012;Langenetal.,2007;Morelleetal.,2013).Identifying hot-momentsofWVCusinglargertemporalperiodsmayprovide importantinformationtoimplementshort-timemitigation meas-uressuchastemporaryroadclosureorspeedreduction(Hobday andMinstrell,2008;Sullivanetal.,2004).Thelackofaggregation periodsformammalsmaystemfromthefactthatthedatasetwas composedmostlybyhighlymobileandgeneralistspecies.These

traitsleadtoamoreuniformdistributionofroadkills,which mini-mizesthechancesofoccurringWVA.

Itshouldbenotedthatbothspatialandtemporalvariationof roadkillsmayberelatedtodifferencesinvehicletrafficduringthe yearorfluctuationsinpopulationabundance(Coelhoetal.,2012; Smith-PattenandPatten,2008).Unfortunately,toourknowledge, suchdatadoesnotexistforourstudyarea.Also,weworkedatthe taxonomiclevelofClass,therebyprecludingmorespecific analy-ses.Byanalyzingatthespecieslevel,suchpatternscouldprobably bemorestableovertime.However,thiswouldrequirealarge vol-umeofroadkilldataforsinglespecies,whichisratherunfeasible andnotpossibleforourdataset.Finally,wechosenottoanalyze scalesgreaterthan2000m,asthecostsofimplementingmitigation measureswouldbecomeexcessive.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.pecon.2017.03.003.

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Beaudry,F.,deMaynadier,P.G.,Hunter,M.L.,2008.Identifyingroadmortality threatatmultiplespatialscalesforsemi-aquaticturtles.Biol.Conserv.141, 2550–2563.

Benjamini,Y.,Hochberg,Y.,1995.Controllingthefalsediscoveryrate:apractical andpowerfulapproachtomultipletesting.J.R.Stat.Soc.B57,289–300. Coelho,I.P.,Teixeira,F.Z.,Colombo,P.,etal.,2012.Anuranroad-killsneighboringa

peri-urbanreserveintheAtlanticForest,Brazil.J.Environ.Manage.112,17–26. Costa,A.S.,Ascensão,F.,Bager,A.,2015.Mixedsamplingprotocolsimprovethe

cost-effectivenessofroadkillsurveys.Biodivers.Conserv., http://dx.doi.org/10.1007/s10531-015-0988-3.

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herpetofaunamortalityonruralhighways.J.Wildl.Manage.71,1361–1368. Malo,J.E.,Suárez,F.,Díez,A.,2004.Canwemitigateanimal-vehicleaccidentsusing

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Imagem

Fig. 1. Location of wildlife-vehicle aggregations (WVA) per year and class, along the 114 km of road surveyed (A) and along the year (B)
Fig. 2. Phi correlations between consecutive years, per class and according to the spatial (A) or temporal (B) unit used to detect WVA.
Fig. 3. Cost-benefit assessment using the relation between the proportion of casualties that could potentially be avoided with the proportion of road (A) or year (B) that would be mitigated

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