Seasonal and circadian biases in bird tracking with solar GPS-tags

19 Pages·2017·1.97 MB·English

RESEARCHARTICLE
Seasonal and circadian biases in bird tracking
with solar GPS-tags
RafaSilva1*,IsabelAfa´n2,JuanA.Gil3,JavierBustamante1,2
1 DepartmentofWetlandEcology,Estacio´nBiolo´gicadeDoñana(EBD-CSIC),Seville,Spain,2 GISand
RemoteSensingLab(LAST-EBD),Estacio´nBiolo´gicadeDoñana(EBD-CSIC),Seville,Spain,3 Fundacio´n
paralaConservacio´ndelQuebrantahuesos,Zaragoza,Spain
*[email protected]
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Abstract
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GlobalPositioningSystem(GPS)tagsarenowadayswidelyusedinwildlifetracking.This
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geolocationtechniquecansufferfromfixlossbiasesduetopoorsatelliteGPSgeometry,
thatresultintrackingdatagapsleadingtowrongresearchconclusions.Inaddition,new
solar-poweredGPStagsdeployedonbirdscansufferfromanew“batterydrainbias”cur-
rentlyignoredinmovementecologyanalyses.WeuseaGPStrackingdatasetofbearded
OPENACCESS
vultures(Gypaetusbarbatus),trackedforseveralyearswithsolarGPStags,toevaluatethe
Citation:SilvaR,Afa´nI,GilJA,BustamanteJ
causesandtriggersoffixanddataretrievallossbiases.Wecomparetwomodelsofsolar
(2017)Seasonalandcircadianbiasesinbird
GPStagsusingdifferentdataretrievalsystems(ArgosvsGSM-GPRS),andprogrammed
trackingwithsolarGPS-tags.PLoSONE12(10):
e0185344.https://doi.org/10.1371/journal. withdifferentdutycycles.Neitherofthemodelswasabletoaccomplishthedutycyclepro-
pone.0185344 gramedinitially.Fixanddataretrievallossrateswerealwaysgreaterthanexpected,and
Editor:AntoniMargalida,UniversityofLleida, showednon-randomgapsinGPSlocations.Numberoffixespermonthoftrackingwasa
SPAIN badcriteriontoidentifytagswithsmallerbiases.Fix-lossrateswerefourtimeshigherdueto
Received:July18,2016 batterydrainthanduetopoorGPSsatellitegeometry.Bothtagmodelswerebiaseddueto
theunevensolarenergyavailablefortherechargeofthetagthroughouttheannualcycle,
Accepted:September11,2017
resultingingreaterfix-lossratesinwintercomparedtosummer.Inaddition,wesuggestthat
Published:October11,2017
thebiasfoundalongthediurnalcycleislinkedtoacomplexthree-factorinteractionofbird
Copyright:©2017Silvaetal.Thisisanopen
flightbehavior,topographyandfixinterval.Morefixeswerelostwhenvultureswereperch-
accessarticledistributedunderthetermsofthe
ingcomparedtoflying,inruggedversusflattopography.Butlongfix-intervalscaused
CreativeCommonsAttributionLicense,which
permitsunrestricteduse,distribution,and greaterlossoffixesindynamic(flying)versusstaticsituations(perching).Toconclude,we
reproductioninanymedium,providedtheoriginal emphasizetheimportanceofevaluatingfix-lossbiasincurrenttrackingprojects,and
authorandsourcearecredited.
deployingGPStagsthatallowremotedutycycleupdatessothatthemostappropriatefix
DataAvailabilityStatement:Allrelevantdataare anddataretrievalintervalscanbeselected.
publiclyavailablefromtheSpanishNational
ResearchCouncil(CSIC)digitalrepositoryatthe
followingURL:http://digital.csic.es/handle/10261/
155119.
Funding:Fundingfortrackingdevicesandfield
Introduction
workwasprovidedbyFundacio´nparala
Conservacio´ndelQuebrantahuesos(FCQ),
ManywildlifemovementstudiesemployGlobalPositioningSystem(GPS)locationdata[1].
GobiernodeArago´n,MinisteriodeMedio
Bothbasicecologyandconservationstudiesuselocationfixesobtainedfromanimalwithtags
Ambiente,Fundacio´nBiodiversidad,ObraSocial
carryingGPSreceivers.Amongothers,therearestudiesonhabitat-selection[2,3],animal
CajaMadrid,Telefo´nicaandLIFE12NAT/ES/
000322.RafaSilvawassupportedbyaPhD behavior[4,5]orhuman-wildlifeconflict[6,7].However,obtainingaGPSfix,andhowreliable
PLOSONE|https://doi.org/10.1371/journal.pone.0185344 October11,2017 1/19
BiasesinsolarGPS-tags
contractfromtheMinisteriodeEducacio´n,Cultura thislocationis,dependsonmanyfactorsthatarenotalwaystakenintoaccountinthesestud-
yDeporte(FPU13-03484).Thefundershadnorole ies.NewGPS-trackingtagstendtogivethousandsoflocationswithveryhighspatialaccuracy.
instudydesign,datacollectionandanalysis,
Theycangivethefalseimpressionofanunbiasedaccountofthebehaviorandwhereaboutsof
decisiontopublish,orpreparationofthe
theanimalswhichcarrythem.But,iffixesarenotobtainedatrandom,morefixesarenotnec-
manuscript.
essarilybetter.Thiscanbespeciallytrickyifanimalbehaviororhabitatusehasaninfluenceon
Competinginterests:Theauthorshavedeclared
theprobabilityoflosingafix.
thatnocompetinginterestsexist.
Onepotentialtrackingbiasisduetothelossoffixesifthereceiveronthetagfailstoreceive
signalsfromaminimumofthreesatellitesduringthelimitedtimetheGPSreceiverison,and
thus,cannotcalculateafix.Thisfact,thatnotallscheduledlocationsareobtained,hassome-
timesbeencalledintheliteratureas“fix-ratebias”[8].Inthisworkwewillusetheterm“fix-
lossrate”(FLR)todescribetherateatwhichscheduledlocationsarenotobtained,calculated
astheinverseoffixsuccessrate,andusethe“fixratebias”torefertoanybiasinthefixingrate
causedbyenvironmental,technical,orbehavioralfactors.Theexistenceofbiasinthefixes
thatareroutinelylossisanimportanteffectthathastobeconsideredintheanalysisofanimal
movement,andsolutionshavetobedesignedtomitigatethem[9].
ManystudiesthathavegainedaninsightintoFLRbiashavebeenbasedonbatteryoperated
GPS-tagsdeployedonterrestrialmammals[8,10–12].TheyhaveconcludedthatFLRbiasis
influencedmainlybyGPSsatellitegeometry,fixinterval(intervalbetweensuccessivefixes),
habitatuse,animalbehavior,orevenGPS-tagpositionandorientation.Itiswellknownthatas
theamountofvisibleskyfortheGPSreceiverdecreases(creatingwhatisknownasapoor
GeometricDilutionofPrecision,orpoor-GDOP)theriskoflosingthefixincreases[13].
Thus,environmentalfactorsthatpreventaclearviewofthesky,suchasruggedtopographyor
canopyclosure,havebeendocumentedashavinganinfluenceonFLR[14,15].Somestudies
haveshownthatasmallerfixintervalsyieldsasmallerFLR[14,16,17].Ithasalsobeendemon-
stratedthatinactiveanimalshavehigherFLRthanactiveones[18].
Althoughthesestudieshaveresolvedmostoftheissuesinfixratebiasinbattery-operated
trackingdevicesusedmainlyinterrestrialmammals,biasinsolar-poweredtagsfrequently
usedforbirdtrackingremainsvirtuallyunexplored.Solardeviceswithrechargeablebatteries
areessentialtotrackbirds,whichrequirelightlong-lastingtags.Birdsalsomoveinathree
dimensionalspaceandtagretrievalisdifficult.Therefore,remotedataretrievalsystemsare
alsoneeded,requiringextrabatteryfordatadownloadcomparedtodeviceswhichlogthedata
andarelatterrecovered.Asaresult,onlydevicesusingsolarrechargeablebatteriesseemable
toofferanadequatesolutiontothisproblem.Torechargethebatterysolartagsrequiresolar
radiation,whichvariesextremelyovertheyear,isaffectedbyweather,andcanbeinfluenced
bydeviceattachment(e.g.becoveredbyfeathers),andbirdbehavior.Researchersareusually
keentogetasmuchdataaspossiblebutintensiveschedulescancompromisetheenergyavail-
ablefortagoperationandcreatedatagaps.Todate,wehaveonlyfoundtwostudiesmention-
ingthenegativeinfluenceofbatterydrainonFLR[17,19].Insummary,althoughthetrendin
tagdevelopmenthasleadtowardsanewgenerationoflightertrackingdeviceswithmoreeffi-
cientpowersolutions,technologyhasnotadvancedenoughyetsothattheriskoflosingfixes
orlosingdataretrievalattemptsinanon-randomwayduetoaninsufficientbatteryperfor-
mancecanbesafelyignored.
Lowbatterycapacityandperformance,andpoorGDOParenotgenerallydirectcausesof
poorGPS-tagperformancebuttheresultingeffectsofacombinationofotherfactorsrelatedto
theelectronics,firmware,andqualityofthecomponents.Forexample,thesuboptimalperfor-
manceoftheunitscanbeaconsequenceofnonoptimalarrangementoftheelectronics.
Antennadesignisoftenconstrainedbythesizeoftheunitsandmightnotbeoptimalcausing
lowantennasensitivityandthisincreasesthetimeneededforsearchingsatellitesandacquiring
ephemerides(increasingbatterydrain).Alowantennasensitivityalsoreducesthenumberof
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BiasesinsolarGPS-tags
satellitesreceived(thusaffectingDOP).Batterychargeisalsodeterminedbytheefficiencyof
thecircuitrycontrollingthesolarrecharging,anddevicesfromdifferentcompaniescanuse
differentcomponentsfortheircircuitry.Alltheseaspectscreatedifferencesbetweentagmod-
elsthatcanbeevaluatedinthelab,buttheeffectofbirdbehaviororhabitatselectionontag
efficiencycanonlybeevaluatedwithrealdeploymentsonbirds.
Besidesfixinterval,thedataretrievalinterval(intervalbetweensuccessivedataretrievals)is
anotherparameterwhichisusuallyscheduledinthetagdutycycle.Mosttagscanstoreon
boardtheGPSlocationsandonlydeletethemoncesuccessfullytransmitted.Dependingon
thestudyobjectives,dataretrievalintervalcanbecriticaltoachievesuccessinthetrackingpro-
gram.Speciesconservationandmanagementprogramsusuallyrequestaquasi-real-time
trackingtopreventorquicklyidentifypotentialmortalityeventsduetopoisoning,accidents
withpowerlinesorillegalhunting[20–22],mainlyatcriticallife-stagessuchasjuveniledis-
persalorduringbreeding[23].Thismeansmanagerswouldaskforfrequentdataretrievals,
every1–2daysintheworstscenario.Argos(www.argos-system.com)PlatformsTransmitters
Terminals(PTTs)hasbeentheonlysystemavailableforanimaltrackingsincethe1970sfor
studiesrequiringworldwidecoverageandinthemid1990sthesystemintegratedGPSreceiv-
ersonthePTTs[24]toobtainhigh-spatial-resolutiontrackingdata.Inthelastdecade,some
GPStagsdeployedonanimalshavestartedtousemobilenetworkdataservicesfordata
retrieval[25].GSM/SMS(GlobalSystemforMobilecommunications/ShortMessageService)
andthemorerecentGSM/GPRS(GeneralPacketRadioServiceforlargerdatasets)have
emergedascheaperalternativestotheArgossystem.Unfortunately,therearestillextensive
areasthroughouttheworld(e.g.areasinAmerica,NorthAsia,Australia,Africa,andpracti-
callyalloceans)withoutGSMservices[26].Inthesameway,dataretrievalsystemsusingradio
modemtechnologyasVHF/UHFornewprotocolslikeZigbeeorBluetoothareasolidalterna-
tive.Theyaresecure,robust,andcheapersystems,andtheyrequirelesspower[27–29]allow-
inghigherdatatransferratesthanArgosorGSM.Howevertheyareonlyappropriatefor
short-rangedownloads,andhence,inadequateforspecieswithunpredictablemovements.
InthispaperouraimistoevaluatetheexistenceofFLRbiasinsolar-poweredGPS-tagsand
determineitscausesusingdatafromtwotagmodelsdeployedonbeardedvultures(Gypaetus
barbatus).Beardedvulturesareparticularlyadequateforthistest.Theyinhabitmountain
rangeswitharuggedtopographythatcreatesdifficultiesforGPSlocation.Thestronglyvari-
ableweatherconditions,andtheseasonalvariationinsolarradiationmakesdifficulttopredict
theperformanceofsolar-poweredGPStagsthatarefrequentlyusedinconservationprojects.
Beardedvulturesrequireslopewindsandthermalupdraftstofly,creatingacircadianpattern
inflightbehaviorthatcouldinfluencethevisibilityofGPSsatellitesforthetags.Weattemptto
findoutwhyGPStagsdeployedonbeardedvultureslosefixesandifthistakesplacewitha
non-randompattern.WeevaluateFLRandtrytoattributeitto"batterydrain"(thetaghasnot
enoughenergytoattemptafix)ortopoorGPSsatellitegeometry(thetagisnotabletocontact
withenoughsatellites,poor-GDOPhereafter).Weevaluatetheinfluenceofotherinteracting
factorssuchasseasonalvariationinsolarradiation,fixinterval,topography,andbirdflight
behavior.OurfirsthypothesisisthatFLRinsolartagsdeployedonbeardedvulturesisnon-
random,neitheralongtheyear,norduringthedailycycle,andisstronglydependentonthe
energyavailabilityforthetag.Accordingly,weexpectthathighcloudcoverageandshorter
daysinwinterwouldproducehigherFLR,becausesolartagsdonotfullyrecharge,andcreate
aseasonalbiasinnumberoffixesacquired.OursecondhypothesisisthatFLRisalsostrongly
influencedbyhabitatuseandbirdbehavior.Differencesintheintensityofflightbehavior
alongthediurnalcycleexposethetagstodifferentrelativesatellite-receivergeometries
(GDOP),andpotentiallyalsotodifferentbatteryrechargeopportunities.Inthisworkwealso
assesstheperformanceoftwodifferentdataretrievalsystemsthathavebeenused(Argosand
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BiasesinsolarGPS-tags
GSM/GPRS).Relatedtoourfirsthypothesis,thelossofdataretrievals,dataretrievallossrate
(hereafterDRLR),shouldfollowthesamepatternasFLRthroughouttheyear,astheenergy
consumptionfordatatransmissionisevengreaterthanforfixcollection.
Materialsandmethods
Ethicsstatements
Thisstudywasconductedasapartofalong-termconservationandresearchprogramleaded
bytheFundacio´nparalaConservacio´ndelQuebrantahuesos(www.quebrantahuesos.org)in
accordancewiththecompetentauthoritiesinthemanagementofthisspecieslistedasendan-
gered(EN)intheNationalCatalogueofThreatenedSpeciesofSpain(R.D.139/2011,BOE
n.46,23thFebruary2011),aswellasinAnnexeIoftheEuropeanBirdsDirective(Directive
2009/147/EC)andSPEC-3category(Europeanthreatenedspecies).Alltheprocedureshave
beenspecificallycarriedoutwithauthorizationoftheNatureConservationAuthorityofthe
GovernmentofAragon,incompliancewiththeregionalDecree45/2003(BOAn.29,25thFeb-
ruary2003)andfollowingtheprotocolsestablishedbytheStrategyforConservationofthe
BeardedVultureinSpain(NationalCommissionforProtectionofNature,4thJune2000).
Speciesandstudyarea
Thebeardedvultureisaspecializedandterritorialscavengerfeedingmainlyonbonesand
inhabitingruggedmountainousareas,inwhichtakesadvantageofslopesoaringinorderto
exploitwithlowenergycoststhelargeareasthatmakeuptheirterritories.Nestsareusually
locatedonremoteoverhungcliffledgesorincaves.Itisanendangeredspeciesremainingina
fewmountainrangesinEurope,Asia,andAfrica[30].InEurope,thelargestbreedingnatural
populationisinthePyrenees(170breedingpairs),withothersmallerpopulationsinCreteand
Corsica.TherehavebeensuccessfulreintroductionprojectsintheAlpsandAndalusianmoun-
tains,wherethespecieswaseradicated.Thespeciesmovementshavebeenstudiedsincethe
1980’swiththehelpofconventionalradiotracking[31],batterypoweredArgosPTTs[32],and
morerecentlysolar-poweredGPStags[23,33–35].Trackingstudieshaveaimedtostudythe
basicmovementecologyofthespeciesaswellastosolveconservationproblemsofwildand
reintroducedpopulations(poisoning,leadintoxication,collisionswithpowerlines,andfood
shortage).
ThestudyareaincludestwodifferentmountainrangesinthenorthoftheIberianPenin-
sula,thenaturalpopulationinthePyreneesandreintroducedindividualsintheCantabrian
Mountains(S1Fig).Bothregionshavearuggedtopography,aseasonalclimate,andvarying
weatherconditions,withelevationsranginguptoapproximately3,300minPyreneesand
2,500minCantabrianMountains.
Fieldprocedures
Between2006and2012,13beardedvultures(threeadults,oneimmature,andninenestlings)
weretaggedwithtwodifferentmodelsofsolarpoweredGPS-tags(S1Table).Allnestlings
weretaggedattheirnests(reintroducedindividualsatthehackingcage)whentheywere
between85and105daysold.Adultsandimmaturebirdsweretrappedwithacannon-netin
vulturerestaurants.Tagsweremountedonbackpack-styleharnessesusing5mmsiliconcord
coveredbyTeflonribbon(BallyRibbonMills,Bally,Pennsylvania,U.S.A.),followingthe
methodologydescribedbyBo¨gel[36],butnotusingtheweaklink.InthePyrenees(0.85˚W
42.51˚N),eightindividuals(threeadults,oneimmature,andfournestlings)wereequipped
withGPS-ArgosPTT-10070gtags,hereafterPTT,(MicrowaveTelemetryInc.,Columbia,
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BiasesinsolarGPS-tags
Maryland,U.S.A.).From2010to2012fiveotherbeardedvulturenestlings(threeinthePyre-
neesandtwointheCantabrianMountains,6.00˚W42.94˚N)wereequippedwithGPS-GSM/
GPRSCTT-11001stGen100gtags,hereafterCTT(CellularTrackingTechnology,LLC.,Somer-
set,Pennsylvania,U.S.A.).Exceptforthedataretrievalsystem,both,CTTsandPTTshavesim-
ilartechnicalcharacteristics(GPSsensor,solarpanels,rechargeablebattery,theystore-on-
boardGPSlocationsuntilsuccessfullytransmitted,etc.).GPStagswereprogramedwithdiffer-
entdutycyclesfollowingtherecommendationofthemanufacturertoobtainthebestperfor-
mance.Oncedeployed,tagscouldnotbereprogrammedremotely.AllPTTswereprogramed
withthesamedutycycle(PTT#1),providingafixevery2hona12hON/12hOFFcycle
from7:00to19:00(CoordinatedUniversalTime,UTC,coincidentinthestudyareawithsolar
time),andadataretrievaleverytwodays.InrelationtoCTTtags,twowereprogramedinthe
firstyear(2010)toprovideafixevery30sfromsunrisetosunset,anddataretrievaleveryday
(CTT#1).Alightsensorswitchedthetagoffduringthenight.Inthesecondyear(2011)asin-
gleCTTwasfitted.Duetopoorperformanceofpreviousschedule,itwasprogramedtopro-
videafixevery15minfromsunrisetosunsetanddataretrievaleverydayifaminimum
numberoflocations,setbythemanufacturer,hadbeenrecorded,withamaximumdata
retrievalfrequencyofonceperday(CTT#2).InpracticeCCT#2scheduleattemptedtransmis-
sioneveryotherday.Inthethirdyear(2012),twoCTTswerefittedandtheywereprogramed
toprovideafixevery15minanddataretrievaleveryday(CTT#3).
Allindividualswerealsoequippedwithconventional20gTW51VHFradio-trackingtrans-
mitters,manufacturedbyBiotrack(Wareham,Dorset,U.K.;4-yrbatterylifeexpectancy),to
allowthebirdstobelocatedincaseofinjuryortechnicalfailureoftheGPS-tag.Birdswere
alsomarkedwithmetalandcolordarvicringsandpatagial/humeraltags.Thetotalweightof
allthemarkswasaround3%ofthebird’sbodymass,belowthegenerallyaccepted5%limit
[37].
Trackingdata
Toavoidproblemswithdaysormonthswithunequalsampling,wediscardedmonthsthat
wereincompleteatthebeginningorendofthetrackingperiodforeachindividual(S2Table).
Forindividualstaggedasnestlings,westartedthetrackingperiodonSeptember1stofthetag-
gingyear,inordertonotincludedataneitherduringthenestingnorthehackingperiods.In
thecaseofindividualstaggedasadultsorimmatures,whichwereusuallytrappedinvulture
restaurantsatanytimeoftheyear,weusedonlydatafromthemonthfollowingthedeploy-
mentdate.TheendofthetrackingperiodforouranalyseswasJune30th,2014forcurrently
activetagsand“lastdataretrieval”dateforinactivetags.OnlydatarecordedduringthePTT
ONcyclewereused(07:00–19:00UTC).Fixesweregroupedin2hintervalsinordertoallow
comparisonsbetweenthetwodifferenttagmodels.Wecalculatedfixanddataretrievalloss
rates(FLRandDRLR,respectively)perindividualasthefractionofscheduledfixesordata
retrievalsthatwerelostforeachdutycycle.Wedifferentiateinbetweenfixeslostduetobattery
drain(BatteryFLR),andfixeslostduetothetagGPSreceiverbeingunabletofindenoughsat-
ellitestocalculatethefix(GeometryFLR),usingtheinformationprovidedbydownloaded
data.Weconsideredafixwaslostduetobatterydrainwhenascheduledfixwasnotrecorded
inthetagdataloggerorwhenatimedregisterwithoutGPS-fixindicatedaninsufficientbat-
teryvoltage“lowbatt”.Regardingfixeslostduetoapoorgeometry,theywerecodedas“9999”
byCTTsandas“nofix”byPTTs.Additionally,acquiredfixesweretaggedbybothtagmodels
withfixquality:2Dwhenonlythreesatelliteshadbeenusedtocalculatethefixandnoaltitude
estimatewasprovided,and3Dwhenfourormoresatelliteswereusedtocalculatethefix.
OnlyCTTsprovidedtheHorizontalDilutionofPrecision(HDOP)foreachfix.Wecalculated
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BiasesinsolarGPS-tags
theeffectivetimelagbetweensuccessivefixesanddataretrievalstoevaluatetheperformance
ofthedifferentdutycycles(S3Table)andcomparedittoprogramedschedules.Birdbehavior
ateachfix(classifiedasperchingorflying)wasestimatedforbothtagmodelsonthebasisof
theinstantaneousGPS-speedprovidedbythetag.Speedthresholdbetweenbothbehaviors
wasestablishedfollowingavisualinspectionofinstantaneousGPS-speedhistogramsof3D-
fixes,taking1.39m/sasthelimitbetweenperchingandflyingfixes.Tagbatteryvoltageand
birdflyingaltitudewerecalculatedfromthevaluesprovidedbybothtagmodelsforeachfix.It
isnotpossibletoknowwherethevulturewasorwhathappenedtotheGPS-tagwhenafixwas
notrecorded,butweassumewecandeducethecausesoflosingfixesfromthequalityinforma-
tionprovidedbyrecordedfixes.
DatarecordedbythetagswereautomaticallyuploadedintoMovebank(www.movebank.
org)withinthestudynamed“BeardedVulture(Gypaetusbarbatus),PyreneesandCantabrian
Mountains”throughCTTGSMandArgoslivefeedsinordertofollowestablishedrecommen-
dationsforanimalmovementdata[38].
Environmentaldata
Wedownloadeddataonmeanmonthlypotentialsolarradiationfromthedigitalclimateatlas
oftheIberianPeninsula[39].Wefirstlycalculatedthe90%-MCP(MinimumConvexPolygon)
foreachindividualusing3D-fixes.ThenweextractedtheradiationvalueswithineachMCP
foreachtag.Elevation(inmetersaboveWGS84ellipsoid)wasdownloadedfromthe30-m
spatialresolutionASTERGlobalDigitalElevationModel(GDEM)v.2[40]toestimatethevul-
tures’flyingaltitudeabovegroundlevel.Elevationdatawasalsousedtoestimatetheterrain
roughness,calculatedasthestandarddeviationoftheelevationwithina500-mbufferaround
each3D-fix.
GPStests
GPStheoryexplainsthatGPSreceiversrequiremoreTimeToobtainaFix(TTF)indynamic
thaninstaticconditions[41].TTFisalsoshorterwhenthescheduledfixintervalisshorter,
becausetheGPSreceiverneedstoreadephemerisandalmanacdatafromeachGPSsatellite
beingtrackedatleastonceperhour.DependingontheGPSreceivertype,collectionofephem-
erisandalmanacdata,cantakefrom30sto3min.BecauseGPSreceiversprogramedwith
shortfixintervals(below1h)canusepreviouslytransmitteddata,theyareabletominimize
TTFmorethanthoseprogramedwithlongfixintervals(above1h).Afirstexploratoryanalysis
ofthedatasetsuggestedthattherecouldbeaninteractionbetweenfixintervalandbirdbehav-
ior(perchingorflying)inFLRbias,becausePTTtagsthathavelongerfixintervals(2h)
recordedahigherfractionofperchingfixesthanCTTtags.Whenthetagismovingandfix
intervalislong,TTFincreasesdramaticallyandthereisahigherprobabilityoflosingafix.We
designedafieldexperimenttotestforaninteractionbetweenfixintervalandinstantaneous
GPS-speed(classifiedasstaticordynamic)inTTF.WeusedaGarminGPSMAP162shand-
heldGPSdevicewiththesamethreefixintervalsasprogramedinthebeardedvultures’tags.
WemeasuredtimesincetheGPSreceiverwasswitchedonuntila3D-fixwithanerrorbelow
5mwasobtained.30TTFmeasurementsweretimedwithastopwatchforeachstate(static
anddynamic)andfixinterval(30s,15minand2h)(n=180)byperformingalternativesta-
tionaryanddynamictests.Stationarytestswerealwaysconductedatthesamepoint(6.56˚W,
37.89˚N)inordertoavoidthebiasproducedbytopography.Dynamictestswerecarriedout
drivingtheGPSonacaronafixed10-kmrouteataspeedof50(km/h).MaximumGPStime-
outwasestablishedas180s.Afterthistime,ifnofixwasachieved,theGPSwasturnedoffand
thefixwastakenaslost.
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BiasesinsolarGPS-tags
Statisticalanalysis
Toestimatethepotentialseasonalandcircadianbiasesinfixesanddataretrievalsattemptswe
fittedGeneralizedLinearMixedModels(GLMMs).WeusedBatteryFLR(fixeslostduetobat-
tery/fixesscheduled),GeometryFLR(fixeslostduetopoorGDOP/fixesscheduled)and
DRLR(dataretrievallost/dataretrievalsscheduled)asresponsevariablesinthemodelswith
“binomial”errorsand“logit”links.TotestfortheexistenceofaseasonalbiasinFLRand
DRLRduetobatterydrain,wefittedaGLMMusingasresponsevariablesBatteryFLRand
DRLR,andaspredictorvariablesthetagmodelandmonth,includingtheindividualasaran-
domfactor.TotestfortheexistenceofacircadianbiasinFLRduetopoor-GDOP,wefitteda
GLMMusingasresponsevariableGeometryFLR,andaspredictorvariablestagmodeland
solartime(HourUTC),includingtheindividualasarandomfactor.Statisticalsignificanceof
predictorswasmadewithanANOVAtest,usingtheChi-squaredtesttoselectamongalterna-
tivemodels.
Todeterminetherelationshipbetweensolarradiationandbatteryvoltage,usingmean
monthlyvaluesforeachindividualtag,weusedlinearregressionanalysis.Theinfluenceof
birdflightbehavior(basedontheinstantaneousGPS-speedclassificationas“perching”or“fly-
ing”)onGeometryFLRwasexaminedwithlinearregressionanalysis.WerelatedHDOPwith
terrainroughnessandvultures’flyingaltitudeforfixesclassifiedas"perching"and"flying"
respectively.Previously,wetestedwithaMann-Whitney’sUtest,iftherewereanydifferences
inmeaninstantaneousGPS-speedvaluesbetweenbothtagmodels.ToanalyzeourfieldGPS
experiment,weusedatwo-wayANOVAtotestfordifferencesinTTFinrelationtofixinterval
andstate(staticanddynamic)andalsoitsinteraction.Toavoidhavinganunbalanceddataset,
weconservativelyusedTTF=180sforthefixesthatwerenotacquiredusingthemaximum
GPStimeout.
AlldataanalyseswereperformedwithRv.3.2.4[42]accessingtomovebankdatastorebyR
package“move”[43].
Results
The13beardedvulturestrackedina7yearperiodfrom2007to2014providedatotalof
83,231GPSfixes(48.1%wererecordedbyCTTsand51.9%byPTTstags).CTTtagsprovided
anaverageof256.3fixespermonthoftracking,whilePTTtagsprovidedanaverage126.6fixes
permonthoftracking(S1andS2Tables).
Trackingefficiency
CCTswereprogramedtoprovide,dependingondutycycle,from2,880(CTT#1)to48
(CTT#3)fixesperday,whilePTTswereallprogramedtoprovide7(PTT#1)fixesperday.Nei-
thertagmodelaccomplishedthistask.Regardingdays-with-fixes,CTTsonlycollectedfixesin
31.88±33.30%(mean±SD)ofthedaysoftracking,providingaFLRof0.93±0.07,while
PTTscollectedfixes85.54±10.67%ofthedays,providingaFLRof0.40±0.12(Fig1and
Table1).GapsbetweenfixeswereusuallylongerandmorefrequentinCTTsthaninPTTs.
Themaximumperiodwithoutfixesrangedfrom12to307daysforCTTs,andfrom7to11
daysinPTTs.Thestandarddeviationofthetimelagbetweensuccessivefixeswas83.65hfor
CTTsand7.68hforPTTs.WithregardtothelocationaccuracyofGPSfixes(estimatedas
thepercentageof3Dfixesfromtotalfixes),CTTsprovidedmoreaccuratelocations(%3D
fixes=88%±9%)thanPTTs(%3Dfixes=77%±6%).
AbetterperformanceondataretrievalwasfoundinPTTs(DRLR=0.20±0.11)than
inCTTs(DRLR=0.89±0.06).Thetimelagbetweensuccessivedataretrievalswascloser
inPTTstotheprogramedschedule(scheduledeverytwodays,meanretrievaltime-
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Fig1.Trackingefficiency,trackingqualityandcausesoffixlossofGPSsolartags.Tagmodels:
CelltracktechGSM-GPRS(CTT)andMicrowaveArgos(PTT).TrackingEfficiency:meanrateofscheduled
fixesthatwereacquired(blue)andlost(red).TrackingQuality:Basedonacquiredfixes(blue),thepercentage
ofrealfixesthatare3Dfixes(solid)versus2Dfixes(hatched).Basedonlostfixes(red),thepercentagethat
werelostduetobatterydrain(norecord,ortaggedas"lowbatt")(solid),andduetopoor-GDOP(recordwith
nolocation,ortaggedas"timeout")(hatched).
https://doi.org/10.1371/journal.pone.0185344.g001
Table1. Fixlossrate(FLR),dataretrievallossrate(DRLR)andperformanceofindividualGPSsolartags.
Individual Dutycycle Dayswithfix(%) FLR %3D Time-lag DRLR Time-lag(days)
max(days) SD(hours) max SD
Carrodilla PTT#1 61 0.66 78 9 13.86 0.46 22 2
Asterix PTT#1 88 0.38 75 8 5.35 0.12 14 1
Goriz PTT#1 91 0.39 75 9 6.95 0.18 14 1
Rover PTT#1 83 0.33 90 8 7.59 0.20 10 1
Eva PTT#1 87 0.45 73 11 8.31 0.21 12 1
Ixeia PTT#1 87 0.44 69 11 8.36 0.19 14 1
Sevil PTT#1 96 0.3 76 7 5.59 0.11 10 1
Maria PTT#1 91 0.26 78 7 5.41 0.11 10 1
PTTmean 86 0.4 77 9 7.68 0.20 13 1
PTTSD 11 0.12 6 2 2.79 0.11 4 0
Deva CTT#1 16 0.99 89 243 65.79 0.85 246 25
Coto CTT#1 7 0.99 96 230 85.19 0.93 230 40
Luisa CTT#2 90 0.88 93 12 8.49 0.93 59 8
Cotiella CTT#3 24 0.82 90 182 62.15 0.80 183 18
Atilano CTT#3 22 0.96 73 307 196.62 0.93 310 49
CTTmean 32 0.93 88 195 83.65 0.89 206 28
CTTSD 33 0.07 9 111 69.27 0.06 94 16
Dutycycle:PTT#1=onefixevery2hona12hON/12hOFFcyclefrom7:00to19:00UTC,Dataretrievalevery2days,CTT#1=onefixevery30sfrom
sunrisetosunset.Dataretrievaleveryday,CTT#2=onefixevery15minfromsunrisetosunset.Dataretrievalonceacertainnumberoffixesarestored,
CTT#3=onefixevery15minfromsunrisetosunset.Dataretrievaleveryday.Dayswithafix(%ofdaysobtainingatleastoneGPSfix),FLR=FixLoss
Rate(fractionofscheduledfixesthatarelost),%3D(%offixesthatareacquiredwiththreeormoresatellitesandhavealtitudeinformation).DRLR=Data
RetrievalLossRate(fractionofscheduleddataretrievalsthatareunsuccessful).FixTime-lag=timelagbetweenconsecutivefixes.RetrievalTime-
lag=timelagbetweenconsecutivedataretrievals.
https://doi.org/10.1371/journal.pone.0185344.t001
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BiasesinsolarGPS-tags
lag=2.44±1.32days)thaninCTTs(scheduledeveryday,meanretrievaltime-lag=10.54±
27.93days).Retrievaltime-lagsrangedbetween10–22daysforPTTsand59–310daysfor
CTTs(Table1).
Seasonalandcircadianbiasesinfixanddataretrievallossrates
Fix-lossrate(FLR)wasingeneralmorenoticeableduetobatterydrain(90%ofthefixeslost
byCTTsand68%ofthoselostbyPTTs)thanduetopoor-GDOP(10%forCTTsand32%for
PTTs)(Fig1).
Seasonalbias. SeasonalanalyseswithGLMMsshowedasignificanteffectofthemonth
andthetagmodelinBatteryFLRandinDRLR(Table2),withmorefixesanddataretrievals
lossesinautumnandwinterthaninspringandsummer(Fig2andS2Fig).BestGLMMsesti-
matedthatBatteryFLRwas4timeshigher(4.29±0.62,mean±SE),andthatDRLRwas
almost4timeshigher(3.73±0.34)inCTTsthanPTTs,duetotheunevenrechargeofthebat-
teryalongtheyear.
Batteryvoltage. Althoughtheincidentmeansolarradiationwasequalforalltags(S3A
Fig),batteryvoltagewasonaveragelowerinCTTsthaninPTTs(S3BFig).Theresultsof
regressionanalysesshowedapositivesignificantcorrelationbetweenmeanmonthlysolar
radiationandmeanmonthlybatteryvoltage(r=0.41,p<0.05,n=156),bothinPTTs
(r=0.68,p<0.05,n=96)andinCTTs(r=0.45,p<0.05,n=60,Fig3).
Circadianbias. CircadiananalyseswithGLMMsshowedasignificanteffectofsolartime
inGeometryFLR.GLMMshighlightedabiasthroughoutthediurnalcycle.Morefixeswere
lostduetopoor-GDOPintheafternoonthaninthemorningandthegreatestnumberwere
lostclosetodusk.ThepatternwassimilarinbothCTTsandPTTs(Fig4Aand4B).Onlythe
timeofdayshowedastatisticalsignificanteffect,withnosignificantdifferencebetweentag
models(Table3).
Terrainroughness. ASpearman’scorrelationtestshowedapositivesignificantcorrela-
tionbetweenterrainroughnessandHDOP(r=0.12,p<0.001,n=7,398)forthefractionof
3Dfixesclassifiedas"perching",andasignificantnegativecorrelationbetweenflyingaltitude
andHDOP(r=−0.15,p<0.001,n=28,451)forthefractionof3Dfixesclassifiedas“flying”.
Flightbehavior. InstantaneousGPS-speedof3Dfixesallowedustodifferentiatebetween
“perching”and“flying”behavior.Thisallowedustoestimatetheeffectofbirdbehaviorin
FLR.Themeanspeedoffixesclassifiedas“perching”was0.01m/s,(n=29,391)whilefor
thoseclassifiedas“flying”21.1m/s,(n=39,711),withnosignificantdifferencesbetweentag
models(U=8976871,p<0.4096).Thecomparisonoffixesclassifiedas“flying”versus“perch-
ing”indicatedadifferentflightactivitytimebudgetinbeardedvulturesaccordingtotag
model.Usingalltrackingdata,CTTscollecteda80%of3D-fixesinflight,whilePTTscol-
lectedonly20%.Thecircadianpatterninflightbehavior,withhigherflightactivityaround
Table2. GLMMsfittedtofixlossrateduetobatterydrain(BatteryFLR)andtodataretrievallossrate(DRLR)toevaluateseasonalbias.
Model Deviance χ2 Df p-value
BatteryFLR~+(1|Individual)Nullmodel 92929.92
BatteryFLR~Month+(1|Individual) 72096.11 20833.81 11 <0.001
Model Deviance χ2 Df p-value
DRLR~+(1|Individual)Nullmodel 3366.57
DRLR~Month+(1|Individual) 3153.18 213.39 11 <0.001
DRLR~Month+Tagmodel+(1|Individual) 3123.4 29.77 1 <0.001
Bestmodels(inbold)wereselectedbyChi-squaredtest.
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BiasesinsolarGPS-tags
Fig2.SeasonaltrackingbiasduetobatterydrainpredictedbytheGLMM.Meanmonthlyregression
coefficients(solidline),withstandarderrorbars.(A)RelativeBatteryFLR=fix-lossrateduetobatterydrain,
and(B)RelativeDRLR=dataretrieval-lossrate.Januarywasfixedasintercept.
https://doi.org/10.1371/journal.pone.0185344.g002
noon,wasapparentforbothtagmodels(Fig4C),butsuggestedadifferentproportionofflying
vs.perchingbehavior.Throughouttheday,bothCTTsandPTTsrecordedahigherpercentage
of3Dfixesatnoonthaneitherduringthemorningorevening(Fig4D).Whenwecompared
%3Dfixesforeach2-hinterval,PTTswereclosertoahypotheticalunbiasedand100%-effi-
cienttagmodel(FLR=0),i.e.,whichmustacquirethesameamountof3Dfixesateach2-h
interval,conformingwiththeregularfixintervalprogramed.
InteractioneffectofGPSspeedandfixinterval. Thetwo-wayANOVAperformedon
thesampleofourfieldexperimentshowedasignificantinteractionbetweeninstantaneous
GPS-speed(classifiedasstaticordynamicstate)andfixinterval(30s,15minand2h)
(Table4).FieldGPStestsdemonstratedthattheeffectofthelongestfixintervalonthefix-rate
biasishigherinadynamictest(whenGPSismoving)thaninstationarytest(Fig5).Our
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