feather mite abundance varies but symbiotic nature …...feather mites (astigmata: analgoidea,...

Ecology and Evolution 201881227ndash1238 emsp|emsp1227wwwecolevolorg

Received1March2017emsp |emsp Revised12November2017emsp |emsp Accepted20November2017DOI 101002ece33738

O R I G I N A L R E S E A R C H

Feather mite abundance varies but symbiotic nature of mite- host relationship does not differ between two ecologically dissimilar warblers

Alix E Matthews12 emsp|emspJeffery L Larkin3emsp|emspDouglas W Raybuck14emsp|emsp Morgan C Slevin1 emsp|emspScott H Stoleson5 emsp|emspThan J Boves1

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2017TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

1DepartmentofBiologicalSciencesArkansasStateUniversityJonesboroARUSA2DepartmentofBiologyTheUniversityofTexasatTylerTylerTXUSA3DepartmentofBiologyIndianaUniversityofPennsylvaniaIndianaPAUSA4DepartmentofForestryWildlifeandFisheriesUniversityofTennesseeKnoxvilleTNUSA5UnitedStatesDepartmentofAgricultureForestServiceNorthernResearchStationForestrySciencesLaboratoryIrvinePAUSA

CorrespondenceAlixEMatthewsDepartmentofBiologicalSciencesArkansasStateUniversityJonesboroARUSAEmailmatthewsalixgmailcom

Funding informationArkansasStateUniversityDepartmentofBiologicalSciencesArkansasGameandFishCommissionArkansasAudubonSocietyTrustPennsylvaniaGameCommissionIndianaUniversityofPennsylvaniaUSDepartmentofAgricultureForestServiceUSDepartmentoftheInteriorFishandWildlifeService

AbstractFeathermitesareobligatoryectosymbiontsofbirds thatprimarily feedon theoilysecretionsfromtheuropygialglandFeathermiteabundancevarieswithinandamonghostspeciesandhasvariouseffectsonhostconditionandfitnessbutthereislittleconsensusonfactorsthatdrivevariationofthissymbioticsystemWetestedhypoth-esesregardinghowwithin-speciesandamong-speciestraitsexplainvariationinboth(1)miteabundanceand(2)relationshipsbetweenmiteabundanceandhostbodycon-ditionandcomponentsofhostfitness(reproductiveperformanceandapparentannualsurvival)Wefocusedontwocloselyrelated(Parulidae)butecologicallydistinctspe-ciesSetophaga cerulea (CeruleanWarbler)acanopydwellingopen-cupnesterandProtonotaria citrea(ProthonotaryWarbler)anunderstorydwellingcavitynesterWepredictedthatfeathermiteswouldbemoreabundantonandhaveamoreparasiticrelationshipwithP citrea andwithinP citrea females and older individualswouldharborgreatermiteabundancesWecapturedtookbodymeasurementsquantifiedfeathermiteabundanceon individualsrsquoprimariesandrectricesandmonitored indi-vidualsandtheirneststoestimatefitnessFeathermiteabundancedifferedbyspe-ciesbutintheoppositedirectionofourpredictionTherewasnorelationshipbetweenmiteabundanceandanymeasureofbodyconditionorfitnessforeitherspeciesorsex(alsocontrarytoourpredictions)Ourresultssuggestthatspeciesbiologyandecologi-calcontextmayinfluencemiteabundanceonhostsHoweverthispatterndoesnotextendtodifferentialeffectsofmitesonmeasuresofhostbodyconditionorfitness

K E Y W O R D S

feathermiteshost-symbiontinteractionsParulidaeProctophyllodidaesymbiosis

1emsp |emspINTRODUCTION

Manyorganismsengageinintimaterelationships(symbioses)withotherspecies and these symbiotic relationships are commonly categorizedasparasiticcommensalormutualisticHoweverdespitesimplestatic

categorizationtheserelationshipsmayactuallyvaryamongcloselyre-latedspeciesandmaybetemporallyorspatiallydynamic(ChamberlainBronstein amp Rudgers 2014 Thompson amp Cunningham 2002)Symbioses can occur on a transitional continuum and theremay beplasticityofthestaticsymbioticcategorizationsdependingoncontext

1228emsp |emsp emspensp MATTHEWS ET Al

(LeungampPoulin2008)Birdsharboravarietyofectosymbiontsincludingfeathermites(AstigmataAnalgoideaPterolichoidea)whosesymbioticrelationshipwith theiravianhostshas recentlybeendebated (Galvaacutenetal20082012Soleretal2012)Feathermitesareobligatoryec-tosymbioticarthropodsthat inhabitthesmallspacesbetweenfeatherbarbsandarethoughttoprimarilyfeedonoilysecretionsfromtheuro-pygialglandwhicharedistributedacrossfeathersbypreening(Proctor2003)Feathermiteshavestreamlinedbodiesandspecializedambulacra(feet) thatallowthemtohold tightlyonto featherbarbulesandresistturbulentairflowduringflight(DabertampMironov1999)

Thespecializeddietaryandmorphologicaladaptationsoffeathermites suggest the strong symbiotic relationship betweenmites andtheir avian hosts However the specific nature of this relationship(positive negative or neutral) and any context dependency of thesymbiosis has not been resolved Thus few generalizations can bemadeaboutfactorsthatdrivevariationinthisrelationshipbothwithinandamongspecies

Mostpreviousworkexploringthisrelationshiphastestedforcor-relationsbetweenmiteabundanceandcurrentphysiologicalconditionForexamplecorrelationsbetweenfeathermiteabundanceandhostbodymassandotherbodyconditionindiceshaveledtoinferencesofbothmutualism(BlancoampFriacuteas2001Lindstroumlmetal2009VillaLeBohecKoopProctorampClayton2013)andcommensalism (BlancoTella amp Potti 1997 Carleton amp Proctor 2010 Davis amp Cornelius2013)Furthermorepreviousstudiestypicallyhaveconcentratedonhowmiteabundancecaninfluenceasinglecomponentofhostcurrentfitness(DowlingRichardsonampKomdeur2001GalvaacutenampSanz2006Galvaacutenetal2012)limitingtheconclusionsthatcanbedrawnaboutthenatureofthesymbiosisThisisalsolimitingbecausealageffectofmitesispossibleandfewstudieshavetakenthenextsteptorelatemiteabundancetofuturehostfitness(reproductiveperformanceandorannualsurvival)whichmaydemonstratehowmitesaffectanindi-vidualoveritslifetimeInfacttoourknowledgeonlyonestudy(PapToumlkoumllyiampSzeacutep2005)hasassessedhowfeathermiteabundancere-latesbothtoreproductiveparametersandannualsurvivaltheyfoundnorelationshipsineithercase

Theseindividualcasesalsohighlightamajorvoidinourunderstand-ingofrelationshipsbetweenfeathermitesandtheirhostsAlthoughanumberofstudieshaveexploredthepotentialfactorsthatarerelatedtovariation inabundanceoffeathermitesonhostswithinaspeciesfew studies have then assessed how those same factors contributetocontextdependencyoftheeffectsoffeathermitesonhostfitnessamongandwithinspeciesAvarietyofamong- (egecologicalaffili-ations)andwithin-speciesfactors (egageorsex)mayberelatedtomiteabundanceandsomemaytheninteractwithmiteabundancetoinfluencehost fitnessAmongspecies somehostsmayhavegreatermite abundances because of their ecological context or life historystrategy(Diaz-Realetal2014Galvaacutenetal2008)whichinturncaninfluencehowmitescanaffectindividualhostfitnessThismaybees-peciallytrueifthereisathresholdatwhichhostingmitesbecomesbur-densome(Galvaacutenetal2008HaribalDhondtRosaneampRodriguez2005)Alternativelyindividualsofsomespeciesmaybeabletosustainanequivalentmiteabundancewithnoeffectsonfitness

Forexample a speciesrsquo nestingecologymay influencebothmiteabundanceandtheeffectsofmitesonhost fitnessas feathermitesaredependentuponthemicroclimateofthehost(andultimatelythehostrsquosenvironment)During thebreedingseasonmuchof thehostrsquosenvironmentisatthenestespeciallyforfemalesInadditionitisatthenestwherefeathermitesprimarilydispersetonewhosts(theoffspringDontildeaetal2017)whichmeansthattheywouldbeevenmoreaffectedbythenestenvironmentastheymovefromhosttohostSpecificallyunderstory dwelling cavity-nesting species may occupy nests thatmakethemmoresusceptibletoparasiticmiteabundancesthantheircanopydwellingopen-cupnestingcounterparts(GalvaacutenampSanz2006)ThisismechanisticallypossibleforseveralreasonsFirstabioticcondi-tionssuchastemperatureandhumiditywithincavitiesintheunder-storymaybemoresuitableformitesandthushostsmayhavegreatermiteabundances(atleastduringthebreedingseason)Thisisbecausethegreatestabundanceofmitesonindividualsoccursatrelativelyhightemperatures(above20degCWilesetal2000)andmanyectosymbiontsincreaseinabundanceasrelativehumidityincreases(MoyerDrownampClayton2002)Furthermoresecondarycavity-nestingspecies(thosethatnest incavitiesthathavebeenmadebyheterospecifics)maybeevenmoresusceptibletoparasiticmiteabundancesbecauseofthepo-tentialformitestoliveinpreviouslyusedcavitiesandtransfertonewhostsapossibilitythathasbeenproposedbutnotyettested(CarletonampProctor2010)Finallyspecieswiththislifehistorystrategy(second-arycavity-nesting)couldalsoincreasetheprobabilityofaforeignmitespeciesbeinghorizontallytransmittedtoanevolutionarilynaiumlvehostandtheresultingincipientspecies-interactionmayfallfurtherontheparasiticsideofthesymbioticcontinuum(JohnsonGrahamampSmith1997LeungampPoulin2008)

Justasinterspecificvariationinecologymayberelatedtoboththeabundanceoffeathermitesandtheireffectsonhostfitnessintraspe-cifictraits(egsexandage)mayalsobeimportantAlthoughvariationinmiteabundancebyhostsexhasbeeninvestigatedbefore(CarletonampProctor2010HamstraampBadyaev2009)noobviouspatternshaveemergedandthereiscurrentlynoclearexplanationastowhythisvari-ationmayexistHere again a speciesrsquo ecological contextmayplay aroleForexampleinspeciesthatexhibittypicalsexrolesfemalesmayharborgreatermiteabundancesthantheirmalepartnersbecausetheyspendmoretimeonthenestlayingandincubatingeggsandbroodingtheiryoungTheymayalsobemorenegativelyaffectedbymiteses-pecially iftheyharbormiteabundancesabovesomethresholdduringthebreedingseasonAgemayalsobeafactorbutthereareconflict-ingpatterns inthe literatureForexample inBarnSwallows (Hirundo rustica)adultshadhigherfeathermiteabundancesthanjuveniles(Papetal2005)Thisresultcanbejustifiedbecausemitestypicallymatureoneeggatatime(Dubinin1951)anditmaytaketimeformitepopula-tionstobuilduponyoungbirdsHoweverDavisandCornelius(2013)foundtheoppositepatternwithyoungerHouseFinches(Haemorhous mexicanus)harboringmoremitesthanadultsInadditionitisunknownhowtheinteractionbetweenecologicalaffiliationageandsexmayin-fluencefeathermiteabundanceorfeathermiteimpactsonhostfitness

In this study we explored how feather mite abundance variedamongspecies(dueinparttodifferingnestingecologies)andwithin

emspensp emsp | emsp1229MATTHEWS ET Al

species (by age and sex) and subsequently how these among- andwithin-speciesfactorsmediatedthenatureofthesymbioticrelation-shipbetween feathermitesand their avianhosts (ie ifmiteshavedifferential effects on hosts) To do so we quantified feather miteabundanceandcorrespondingfitness(reproductionandsurvival)fromindividualsbelongingtotworelativelycloselyrelatedNewWorldwar-blerspecies(familyParulidae)thatdiffer innestingecology(oneisacanopy dwelling open-cup nester and one an understory dwellingsecondarycavitynester)Wetestedtwomainhypothesesrelatedto(1) the factors that explainvariation inmite abundance among andwithinspeciesand(2)therelationshipbetweenmiteabundanceandhostbodyconditionandfitnesscomponentsWefirsthypothesizedthatmiteabundancediffersamongandwithinspeciesWepredictedthatmiteswillbemoreabundanton(a)anunderstorydwellingcavity-nestingspeciesandwithinspecieson(b)femalesand(c)olderbirdsSecondwehypothesized that the relationship betweenmite abun-danceandbodyconditionandhostfitness(reproductiveperformanceandsurvival)isalsocontingentonseveraloftheseamong-andwithin-speciesfactorsWepredictedthatrelationshipsbetweenmiteabun-danceand(a)bodyconditionand(b)hostfitnesswillbemorestronglynegative (iemiteswillhaveamoreparasiticeffect) forunderstorydwelling cavity-nesting species than for canopydwelling open-cupnestersandevenmoresoforfemalecavitynestersthanforconspe-cificmalesWe evaluated both reproduction and annual survival ofindividualsandwequantifiedfeathermiteabundanceusinganovelobjectivesystemthatincludedallprimaryandrectrixfeathers

2emsp |emspMATERIALS AND METHODS

21emsp|emspAvian study species

We focused our efforts on two relatively closely related songbirdsin the family Parulidae (Lovette etal 2010) Protonotaria citrea (ProthonotaryWarbler)andSetophaga cerulea(CeruleanWarbler)ThelifehistoriesofthesespeciesoverlapinmanyrespectsBothspeciesarehighlyinsectivoroussexuallydimorphicsociallymonogamousandnestinforestsoftheeasternUnitedStates(BuehlerHamelampBoves2013 Petit 1999)Moreover these species are both NeotropicalndashNearctic migrants However these species differ in two importantecologicalfactorsP citreaisoneoftwowarblerspeciesthatnestincavitiesintheunderstorylt4mabovetheground(Petit1999)S ceru-leabuildopen-cupnestshighinforestcanopiestypicallygt15mabovetheground(Buehleretal2013)Themoltscheduleforthefeathersthatweassessed(primariesandrectrices)isnearlyidenticalforbothspecies they both typically molt these feathers postbreeding butbeforefallmigration(oroccasionallyduringearlystagesofmigrationinNorthAmericaPyle1999BovesFairhurstRushingampBuehler2016ErikJohnsonAudubonLouisianapersonalcommunication)

22emsp|emspStudy areas

Weconductedour researchduring thebreeding seasonsof 2015ndash2016atprimaryfieldsitesthatwerelocatedinareaswherewehad

already been conducting unrelated research on these two warblerspecies We then augmented these locations with secondary fieldsitesduringthefollowingbreedingseason(in2017)ForP citreaourprimary fieldsitewas ina southernportionof theirbreeding rangein100-haofeast-centralArkansasUSAintheDaleBumpersWhiteRiver National Wildlife Refuge (34deg2primeN 91deg1primeW Figure1) wheremalesandfemalesbotharrivebylateAprilForS ceruleaourprimaryfieldsitewasinthenorthernportionoftheirbreedingrangein500-ha of northwestern Pennsylvania USA along the Allegheny Riverextending onto the Allegheny Plateau (41deg7primeN 79deg2primeW Figure1)where males and females both arrive by late May These primarylocations from which we collected data are clearly geographicallyseparatedbutthesespeciesonlyspendtwotofivemonthsoftheirfullannualcycleintheselocations(Buehleretal2013Petit1999)Evidencefromdataobtainedbylight-levelgeolocationsuggeststhatduringtherestoftheyear(nonbreeding)manyindividualsfromthesetwopopulationsspendsixtoninemonthsrelativelyclosetoonean-otherinnorthernColombia(TonraetalinreviewTJBandDWRunpublisheddata)ConverselyS ceruleathatbreedclosertoArkansasappeartooverwintermuchfurthersouthwestalongtheAndesmoun-tains(withinornearPeruDWRunpublisheddata)Thuswhencon-sideringthefullannualcyclethebreedingpopulationsutilizedforthisstudylikelyrepresentgreatergeographicsimilarityforamuchlongertimeperiod thanhadweused individualswhosebreeding locationswerecloserDespitethislikelyoverlapofnonbreedinglocationswefurtheraddressedthepotentialconfoundingfactorofgeographybyaddingsecondaryfieldsitesforbothspecies(in2017)Attheseloca-tionswecollecteddataonfeathermiteabundancebutduetologisti-calconstraintswereunabletoincludereproductiveorannualsurvivaldataintheseareasForS ceruleaoursecondaryfieldsitewasinthesouthernportionof their breeding range in north-centralArkansasUSA inBuffaloRiverNationalPark (36deg0primeN92deg6primeWFigure1) andinsoutheasternMissouriUSAalongtheElevenPointRiver inMarkTwainNationalForest (36deg7primeN91deg2primeWFigure1)ForP citreaoursecondary field site was in the northern portion of their breedingrangeinsouth-centralWisconsinUSAinAvonBottomsStateNaturalArea(42deg5primeN89deg3primeWFigure1)

23emsp|emspCapturing birds

WecapturedbirdsatbothprimaryandsecondaryfieldsitesTocap-turemalesofbothspeciesweplacedspeakersandadecoyinvegeta-tiononbothsidesofamistnetandthenbroadcastedaudiotracksofeachspeciesrsquo songorcallTocapture femaleP citreaweheldamesh bag over nest cavity openings early in the incubation periodandflushedthefemale intothebagOncecapturedwebanded in-dividualswithUnitedStatesGeologicalSurveyaluminumbandsandauniquecombinationofplasticcolorbands (toallowfor identifica-tionofindividualswithoutrecapture)Recordeddataincludedsex(viaplumageandbroodpatchcloacalprotuberance)age(viaplumageormoltlimitsSYsecondyearASYaftersecondyearPyle1999)mass(usingadigitalscale)andwingchord(usingawingrule)AllindividualswerecapturedeitherjustbeforeorduringthenestingperiodBanding


andanimalhandlingprocedureswerepermittedandapprovedbytheUSGSBirdBandingLabPermit23877andArkansasStateUniversityIACUCProtocol638636

24emsp|emspFeather mite identification

Todocumentfeathermiteidentitieswecollectedasmallnumberofmitesfromtheprimaryandrectrixfeathersofbothwarblerspecies(fromindividualsnotincludedinthisstudy)Wesortedmitemorphos-peciesusingadissectingmicroscopeandslide-mountedrepresenta-tivespecimensthatweexaminedusingacompoundmicroscopeWeused Gaud and Atyeo (1996) to identify specimens to genus andDrs Sergey V Mironov (Zoological Institute Russian Academy ofSciences) andHeather C Proctor (University of Alberta) confirmedidentification

25emsp|emspMeasuring mite abundance

Toquantifymiteabundanceweextendedthewingandtailofeachbirdandusedadigitalcamerawithamacro-lenssettingtotakephotosoftheventralsideofbothwingsandbothsidesofthetail(Figure2)We reviewedeachphoto for clarity andcomparedwith thebird inthefieldtoconfirmthatallindividualfeathermitesacrosseachentirefeatherwerevisiblebeforereleasingeachbirdTheprocesstookanaverageoffiveminWeuploadedphotostoacomputerandAEM

censusedthemites(iecountedeveryindividualfeathermite)onall18primaries(nineoneachwing)andall12rectrix(tail)feathers

26emsp|emspReproductive performance

Atprimaryfieldsitesduringthebreedingseasonof2015welocatednestsof individualsusingbehavioralcues (mainlynestbuilding)andmonitoredthemevery1ndash3daysuntilfledgingorfailureForP citreaweprimarilyuseddigital inspectioncamerasequippedwith flexiblefiberopticcablesthatcanbemaneuveredintocavitiesWerecordednestcontentinformationateachnestincludingnumber(andspeciesbothspeciescanbebroodparasitizedbyMolothrus ater)ofeggsnest-lingsand fledglingsWeconsiderednestsactivewhenge1hosteggwaspresentForS ceruleanestcontentswereunabletobeexamineddirectly until nestlingswere visible thereforewe considered nestsactivewhenweobservedthefemaleincubatingbroodingorparentsprovisioningyoungOncenestlingsnearedfledgingage(10to11daysforbothspecies)wemonitoredallnestsdailytoensurewewereabletoaccuratelydeterminenestfate(failureorfledging)SpottingscopesallowedformonitoringandaccuratecountingofS ceruleanestlingsas they neared fledging ageAfter presumed fledgingoccurredwesearchedthevicinityaroundnestsforjuvenileactivitytoconfirmpu-tativenestfateandtoestimatethenumberoffledglingssuccessfullyproducedFornestsurvivalpurposesweconsideredanestsuccessfulifitproducedge1fledgling

F IGURE 1emspMapofprimary(circles)andsecondary(triangles)studysitesintheeasternUnitedStatesThecolorsrepresenteachhostspecies(yellowProtonotaria citreablueSetophaga cerulea)ThismapwascreatedwiththeRpackageldquoggmaprdquo(KahleampWickham2013)


27emsp|emspApparent annual survival

Duringthe2016breedingseasonwereturnedtoprimaryfieldsitestoattempttoresightallindividualsthatweremarkedthepreviousyearFormaleswevisitedeachterritoryge3timesandallareaswithin~500mofeachterritoryandusedsong-playbacktolureallmalesintoviewInadditionweusedsong-playbacktolureallmalesthatwereheardvocal-izingwithinthegreaterstudyareasintoview(manyfrommuchgreaterthan500mfromamarkedbirdrsquos territory)We investigatedallprevi-ous nest locations to also assist in finding returningP citrea females Bothspecieshaverelativelyhighsitefidelity(Bovesetal20142016McKim-LouderHooverBensonampSchelsky2013)andgivenourlevelofresightingeffortandknowledgeofthesespeciesweareconfidentourmethodscloselyandreasonablyapproximatedannualsurvival

28emsp|emspStatistical analyses

281emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age

Generalizedlinearmodels(GLMs)werebuilttoevaluatehowfeathermiteabundancediffersbyspecies(withafocusonnestingecologyPrediction1a)sex(Prediction1b)andage(Prediction1c)andifanytwo-wayinteractions()existusingdatacollectedfrombothprimaryand secondary field sites For this initialmodeling attemptwealsoincluded the potentially confounding variables of date of capturetheyearofcapture(2015or2017)andregionofcapture(northor

south) as fixedeffectsWe removed interactions thatwerenonsig-nificantandthenestimatedstatisticsfromamodelthatincludedtheconfoundingvariables listedaboveTocorrectforoverdispersionofthedataweconstructedGLMswithaquasi-Poissonerrorstructureandlogarithmiclink

If from this initialmodeling attempt species (or any interactionwithspecies)wasanimportantpredictor(Prediction1aα=005)weseparatedspeciesandassessedfactorsforwithin-speciesdifferencesinmiteabundance(Prediction1bsexPrediction1cageandasex-age interaction) and included the confoundingvariables of date ofcaptureandregionofcaptureasfixedeffectsWedidnotincludeyearinmodelswithspeciesseparatedbecauseregionandyearofcapturewereperfectlycollinearwithinspecies(egeveryS ceruleacaughtin2017wasfromthesouthernportionoftheirbreedingrange)Againweremovedinteractionsthatwerenonsignificantandestimatedsta-tisticsfromamodelthatincludedtheconfoundingvariableslisted

282emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex

Weusedavarietyofstatisticalmethodstoevaluatetherelationshipsbetweenmite abundance (predictor) andbody condition and fitness(responses)forindividualsthatwefollowedfrom2015to2016(atpri-mary field sitesonly)Wecompared inferencesbetweenandwithinspeciesbybuildingseparatemodelsforeachspeciesandsex(forP cit-rea)We used thismethod rather than simply including interactionsbetweenmiteabundanceandspeciessexbecausewewereinterestedinthemoresubtledifferencesinthedirectionalityandorstrengthoftherelationship(betweenspeciesandbetweensexeswithinspecies)

283emsp|emspPrediction 2a The relationship between mite abundance and body condition will be more parasitic for the cavity- nesting species and within this species females

To estimate body condition we regressed mass on wing lengthandthenused the resulting residualsasaproxy forbodycondition(Schulte-HosteddeZinnerMillarampHickling2005)ForeachspeciesandbothsexesinP citreaGLMswereconstructedandweincludedthepotentiallyconfoundingvariablesofcapturedateandageinthemodelsasfixedeffectsinthemodelsWeusedanormaldistributionandidentitylinkWealsotestedforaquadraticrelationshipbetweenmiteabundanceandbodyconditionbecausesomeevidencesuggeststhatahormeticnonlinearrelationshipmayexist(Galvaacutenetal2008)

284emsp|emspPrediction 2b The relationship between mite abundance and fitness will be more parasitic for the cavity- nesting species and within this species females

ForreproductionweusedtheNestSurvivalmoduleinProgramMARK(DinsmoreWhiteampKnopf2002WhiteampBurnham1999)toevaluatetherelationshipbetweenmiteabundanceanddailynestsurvivalforeach

F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph


speciesandsexAkaikersquosinformationcriterion(correctedforsmallsamplesizeAICc)wasused tocomparecandidatemodels toournullmodelswhich forP citrea includednest type (naturalorartificial)presenceofbroodparasitismageofparentandgeolocatorstatus(ifageolocatorhadbeendeployedpriortothecompletionofthenest)ascovariatesandforS ceruleaincludedonlytheageoftheparentWeincludedthevariableofgeolocatorbecauseforanunrelatedstudygeolocators(typicallylt3ofbodymass)wereattachedto18P citrealateinthebreedingseason(afterall firstbroodswerecomplete)P citreanests that faileddueto flood-ingwereexcludedfromanalysesasthisisastochasticeventunrelatedtoanyeffectmitesmayhaveWithineachsexforindividualsthathadgt1nestingattemptduringthebreedingseasononenestwasrandomlychosentoincludeinanalysestomaintainindependenceAquadraticre-lationshipbetweenmiteabundanceandnestsurvivalwasalsoexamined

TofurtherassesspotentialrelationshipsbetweenmiteabundanceandreproductionGLMswerebuiltforeachspeciesandsextoevaluatethere-lationshipbetweenfeathermiteabundanceandthenumberoffledglingsproducedP citrea can produce two (rarely three) broods Becausewewantedtobestcapturetheentirereproductivehistoryofeachindividual(ratherthanselectingarandomnest)butwewereunabletofollowalargeenoughsampleofbirdstobeconfidentoftheirseasonalfecundityweinsteadcomparedtheaveragenumberoffledglingsproducedperparentmonitoredduringtheseason(asopposedtoincludingallnestswithindi-vidualbirdIDasarandomvariableforwhichthemodelswouldnotcon-verge)Thepotentiallyconfoundingvariablesofnesttype(naturalcavityorartificialnestbox)age(secondyearoraftersecondyear)presenceofbroodparasitismandgeolocatorstatuswereallincludedasfixedeffectsinthemodelsforP citreaandagealonewasincludedasafixedeffectinthemodelforS ceruleaAPoissondistributionwithlogarithmiclinkwasusedforthisanalysisbecausethedatadidnotfollowanormaldistributionandcouldnotbenormalizedAquadraticrelationshipbetweenmiteabun-danceandnumberoffledglingswasalsoexamined

ForannualapparentsurvivalGLMswerebuiltforeachspeciesandsextoevaluatetherelationshipbetweenfeathermiteabundanceandapparent annual survival status (yes or no) and the potentially con-foundingvariablesofgeolocatorstatus(forP citrea)andagewerein-cludedasfixedeffectsinmodelsAbinomialfamilyandlogitlinkwereusedforthisanalysisAquadraticrelationshipbetweenmiteabundanceandapparentannualsurvivalwasagainexaminedAllstatisticalanaly-seswiththeexceptionofnestsurvivalanalysiswereperformedusingtheRpackageldquolme4rdquo(BatesMaumlchlerBolkerampWalker2014RCoreTeam2016)andallgraphicswerecreatedwiththeRpackageldquoggplot2rdquo(Wickham2009)Allmeansarereportedplusmnonestandarderror

3emsp |emspRESULTS

In 2015we captured 18 S cerulea (17males and one female) and92P citrea(42malesand50females)atprimaryfieldsitesIn2017wecaptured11S cerulea (allmales) andnineP citrea (allmales) atsecondary field sites Total mite abundance (primaries and rec-tricescombined)onindividualbirdsrangedfromtwoto2254mites(x=436plusmn44mitesperindividual)


Mites fromboth feather tractsonbothhost speciesweremorpho-logicallyverysimilarTheyareallinthesamesubfamily(AnalgoideaProctophyllodidaePterodectinae)andthesamegenus(Amerodectes) Geneticdata(fromtheCOIgene)suggestthatP citreawingandtailmitesareofthesamespeciesbutareadifferentspeciesfromS ceru-leawingandtailmiteswhichincludedtwohaplotypesofanotherun-describedspecies(allareintheprocessofbeingdescribedMatthewsetalinpress)


Specieswasa significantpredictorofmiteabundancewithS ceru-lea harboring significantly more mites than P citrea (Prediction 1aS cerulea 1137plusmn113mitesP citrea 235plusmn20mites t121=minus737plt001Figure3a)Whilespeciesagewasasignificantpredictorinthis initialmodeling attempt (t121=minus255p=01) the confoundingvariablesofdateof capture (t121=minus0921p=36) yearof capture(t121=052p=60)andregionofcapture(t121=158p = 12) were all nonsignificantpredictorsS cerulea harboredmoremitesoverallbut particularly so on rectrices (S cerulea 997plusmn91 mites on rec-trices P citrea 185plusmn17 mites on rectrices t121=minus742 plt001Figure3b)Setophaga ceruleaalsoharboredmoremitesonprimaries(S cerulea170plusmn30mitesonprimariesP citrea50plusmn7mitesonpri-mariest122=minus434plt001Figure3b)

Becausespeciesandspeciesagewereimportantpredictorsintheinitialmodelingattemptwethenseparatedspeciesandassessedfac-torsforwithin-speciesdifferencesinmiteabundanceForP citreasex-agewasnotsignificant(t94=minus171p=09)soweremoveditfromthefinalmodelForP citreamiteabundancedidnotdifferbetweensexes(Prediction1bmales248plusmn32mitesfemales221plusmn24mitest95=minus011p=91)butitdiddifferbetweenageclasseswitholderbirds harboringmoremites thanyounger birds (Prediction 1cASY278plusmn30mites SY 162plusmn21mites t95=minus281p=006 Figure4)Theconfoundingvariablesof region (t95=065p=52)anddateofcapture(t95=minus103p=31)werebothnotsignificantBecauseonlyoneS ceruleafemalewascapturedweexcludedher(aswellassexandsexage)fromanalysesThusforS ceruleamalesmiteabundancedidnotdifferbetweenageclasses(Prediction1cASY1102plusmn132mitesSY1253plusmn189mitest25=054p=59)Theconfoundingvariablesofregion(t25=131p=20)anddateofcapture(t25=minus019p = 85) werebothnotsignificantinthemodelforS ceruleamales


Therewasnorelationship(allpgt19)betweenfeathermiteabun-dance (linear or quadratic) and body condition for either speciesor sex when including age and date of capture as fixed effects(Table1)


Atprimaryfieldsitesin2015welocatedandmonitored61nestsforP citreaat24nestswecapturedboththemaleandthefemaleat26nestsweonlycaptured the femaleandat11nestsweonlycapturedthemaleWelocatedandmonitoredfivenestsforS cerulea malesMiteabundancewasunrelatedtodailynestsurvivalforbothspeciesandbothsexeswithinP citreainallcasesthenullmodelwaseitherthebestfitmodelorexplainedpatternsequallyaswellasthebestfitmodel(Table2)Miteabundancewasalsounrelatedtotheav-eragenumberofyoungfledgedforbothspeciesandsexes(allpgt06Table1) Finally mite abundancewas unrelated to apparent annualsurvivalofP citreaforbothsexes(bothpgt34)aswellasforS cerulea males(p=14Table1)

4emsp |emspDISCUSSION

Thenatureoftherelationshipbetweenfeathermitesandtheirhostshas recentlybeendebatedandpreviousstudieshave led tooppos-ingconclusionswhilefactorsthatexplainthisvariationremainmostlyunstudiedHereweusedtwocloselyrelatedbutecologicallydistinctNeotropicalndashNearctic migratory wood-warblers to test hypothesesrelatedtofactorsthatmayexplainvariationin(1)feathermiteabun-danceand(2)therelationshipsbetweenfeathermiteabundanceandhostfitness

Feathermiteabundancedifferedbetweenthetwospeciessup-portingourfirsthypothesisHoweveritwasintheoppositedirectionofourPrediction1aasS ceruleaharboredmorefeathermitesthanP citreaThereareavarietyofnonexclusiveexplanationsforwhyS ce-ruleaharboredgreatermiteabundancesalthoughallwillrequiremorestudyinordertoprovidestrongsupportEcologycouldhaveaffectedmiteabundancesbothdirectlyand indirectlyBothonbreedingandwinteringgroundsS cerulea live in theoverstorycanopyof forestswhile P citreaoccupytheforestunderstoryThesemicrohabitatsdifferbymany abiotic factors including temperature andhumiditywhichcoulddirectly affect the ability ofmites to surviveor reproduceontheirhosts(Meleacutendezetal2014Wilesetal2000)Itisalsopossiblethatbecausecanopyspeciesmaybeexposedtoharsherenvironmen-tal elements (eg rainwind and fluctuating ambient temperatures)thanunderstoryspeciestheymayneedtopreenmoreoftentomain-tainfeatherconditionthusprovidingmoreuropygialoilformitestoconsume(HensonGalushaHaywardampCushing2007)Differencesassociatedwith thegeographic locationsofour studyareasdidnotappeartobeinfluentialindrivingthespeciesdifferencesasS cerulea frombothregionswereinfestedwithmuchgreaternumbersofmitesthanP citreaineitherregionHoweverabroad-scalestudyinvolving

F IGURE 3emsp (a)TotalaveragefeathermiteabundancedifferedbetweenspeciesSetophaga cerulea (n=29)andProtonotaria citrea (n = 101 plt001)acrossbothcaptureyearsandfieldsitesErrorbarsrepresentplusmn1standarderror(b)TotalaveragefeathermiteabundancebyspeciesandfeathertractS cerulea (n=29)harboredmoremitesthanP citrea (n=101)acrossbothcaptureyearsandfieldsitesonbothfeathertractsparticularlysoontherectrices(plt001)butalsoontheprimaries(plt001)Errorbarsrepresentplusmn1standarderror

F IGURE 4emspAveragefeathermiteabundancedifferedbetweenageclasses(ASYaftersecondyearSYsecondyear)inProtonotaria citrea (n = 101 p=006)acrossbothcaptureyearsandfieldsitesErrorbarsrepresentplusmn1standarderror


TABLE 1emspSummaryofresultsfromlinear(L)andquadratic(Q)generallinearmodelsdescribingtherelationshipbetweenfeathermiteabundanceandbodyconditionoffspringfledgedand

apparentannualsurvivalbyeachhostspecies(S

etop

haga

cer

uleaandP

roto

nota

ria c

itreafromprimaryfieldsites)andsex(maleandfemale)Otherconfoundingfixedvariablesthatwereincluded

ineachmodelarealsolistedundertherespectivemodelTheseincludeddateofcapturenesttype(naturalorartificial)presenceofbroodparasitismageofindividualandgeolocatorstatus(ifa

geolocatorhadbeendeployedpriortothecompletionofthenest)Significantresults(α=005)areboldface(onlyseeninconfoundingeffects)

Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Bodycondition(L)

Totalmites

lt0001plusmnlt0001

t = 0

38

117

1lt0001plusmnlt0001

t = 0

44

3866

ltminus0001plusmnlt0001

t=minus074

4446

Julian

001plusmn0008

t=206

1106

lt0001plusmnlt0001

t=006

3895

minus0006plusmn0007

t=minus083

444

1

Age

023plusmn015

t=156

111

5minus006plusmnlt019

t=minus030

3876

minus012plusmn026

t=minus046

4465

Bodycondition(Q)

Totalmites


t=minus097

1036

0001plusmnlt0001

t = 1

34

3719

lt0001plusmnlt0001

t=064

435

2

Totalmites2

lt0001plusmnlt0001

t = 1

11

1029

lt0001plusmnlt0001

t=minus127

372

1ltminus0001plusmnlt0001

t=minus096

433

4

Julian

001plusmnlt0001

t = 2

17

1006

lt0001plusmn0004

t=009

3792

minus0006plusmn0007

t=minus089

433

8

Age

015plusmn016

t=097

103

5minus0004plusmn020

t=minus002

3798

minus015plusmn027

t=minus056

435

8

Offspringfledged(L)

Totalmites

ltminus0001plusmn0001

Z=minus029

37

7lt0001plusmnlt0001

Z=129

2919


Z=minus186

4306

Nesttype

mdashmdash

mdashmdash

minus006plusmn021

Z=minus033

297

4006plusmn016

Z =

042

4367

Age

minus099plusmn068

Z=minus147

31

4059plusmn023

Z=260

290

09015plusmn017

Z=092

4336

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2999

minus215plusmn059

Z=minus37

43lt

001

Geolocator

status

mdashmdash

mdashmdash

017plusmn032

Z =

055

295

8018plusmn022

Z =

083

434

1

Offspringfledged(Q)

Totalmites

0009plusmn0007

Z=146

21

4lt0001plusmn0001

Z =

004

2897

lt0001plusmnlt0001

Z=094

423

5

Totalmites2


Z=minus159

21

1lt0001plusmnlt0001

Z=046

2864


Z=minus160

421

1

Nesttype

mdashmdash

mdashmdash

minus009plusmn022

Z=minus045

2865

007plusmn022

Z =

047

4264

Age

minus0002plusmn0008

Z=minus031

27

5057plusmn023

Z=246

280

1015plusmn017

Z=092

4236

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2899

minus22plusmn059

Z=minus367

42lt

001

Geolocator

status

mdashmdash

mdashmdash

019plusmn032

Z=061

285

4007plusmn016

Z =

080

424

2

Survival(L)

Totalmites

minus0003plusmn0002

Z=minus148

141

40002plusmn0002

Z=096

383

4lt0001plusmn0002

Z=minus002

4598

(Continues)


multiplehostspeciesfoundacross latitudinalclineswillbeuseful indetermining howmuch geography (directly or indirectly) influencesmiteabundancesespeciallyincomparisonwithotherfactorssuchasecologyphylogenyandevolutionaryhistory(bothwithinandacrosshostspecies)

Anotherpossibleexplanationforthevariationinmiteabundancesbetween species is behavioral particularly related to nestmaterialsselectedbythesespeciesThereisevidencefromothercavity-nestingspecies(Sturnus vulgarisandCyanistes caeruleus)thatsomegreennestmaterials (mainly angiosperms) that P citrea use in nest lining maybetoxictocertain invertebratesandthusreduceectosymbiont load(DubiecGoacuteźdźampMazgajski2013)Setophaga ceruleararely ifeverusegreenmaterialsintheirnestbuilding(Buehleretal2013TJBpersonal observation) This idea could be tested experimentally byaddingorremovingmoretoxic(toectosymbionts)greenmaterialsfromnestsofP citreaandassessingmiteabundanceamongtreatments

In other studies a strong morphological predictor of feathermiteabundanceisuropygialglandsizebothwithinandamongavianspecies (Galvaacuten etal 2008 but see PapVaacutegaacutesi OsvaacutethMuresanamp Barta 2010) However it is not a good explanation in this caseWe measured the surface area of uropygial glands from a sampleofmalebirdsof each speciesS cerulea actually had smaller uropy-gial glands (P citrea =240plusmn04mm2 S cerulea =190plusmn03mm2) which isexpectedgiven that theyaresmalleroverall (bodymassofP citrea=1411plusmn008gS cerulea=971plusmn007g)Itisalsopossiblethatchemicalcompositionofuropygialglandoilmaydifferbetweenspecies promoting different abundances of feather mites (Haribaletal2005)Furtherinvestigationsofspecies-specificanatomicalandbiochemicaltraitswillbenecessarytodecipherwhatproximatemech-anismscouldinfluencevariationinfeathermiteabundance

Relatedtofeathermiteabundancewithinspeciesourresultspar-tiallysupportedoneprediction(withrespecttoage)andrefutedtheother(withrespecttosex)AspredictedolderP citreaofbothsexesharboredmoremites than their younger counterparts For P citreaolderbirdsmayhavesimplyhada longeramountoftimetoacquiremites (andformitestoreproduce)thanyoungerbirdsTheseresultsareconsistentwiththepreviousstudiesofBarnSwallows(BlancoampFriacuteas2001Papetal2005)butinconsistentwithresultsofHouseFinches(DavisampCornelius2013HamstraampBadyaev2009)furthersuggesting that speciesbiologyorecological contextarepotentiallyimportantfactorsinexplainingvariationamongfeathermitestudiesWefoundnodifferenceinfeathermiteabundancebetweensexes(ofP citrea)However given our finding thatP citrea harbor lessmitesthanS ceruleaitisnotunexpectedIfcanopyopen-cupnestingspe-cies are in generalmoreprone to greatermite abundances futurestudiesshouldcomparemiteabundancesbetweensexesofS cerulea andotherspeciesofbothcanopyandunderstoryspecies

Althoughmiteabundancevariedbothbetweenandwithinspeciesthesepatternsdonotseemtoreflectdifferentialeffectsofmitesonhost body condition reproductive performance or apparent annualsurvival as abundancewas unrelated to any of themetrics testedOverall these results suggest a commensal relationship betweenfeathermitesandthesetwospeciesasotherstudieshavealsofound

Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

384

2192plusmn099

Z=194

450

5

Age

minus082plusmn167

Z=minus049

1463

141plusmn094

Z=149

381

4189plusmn075

Z =

253

450

1

Survival(Q)

Totalmites

minus0009plusmn0007

Z=minus126

132

1lt0001plusmn0006

Z =

018

378

5lt0001plusmn0006

Z=016

448

7

Totalmites2

lt0001plusmnlt0001

Z=092

1336


Z=019

378


Z=minus018

4486

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

374

2192plusmn099

Z=194

440

5

Age

minus176plusmn228

Z=minus077

134

4137plusmn097

Z =

037

3716

188plusmn075

Z=249

440

1

TABLE 1emsp(Continued)


(Dowlingetal2001Galvaacutenetal2012)Thismayreflectthatthesefeathermites are simply consuming aminimal amount of uropygialoilwhichhas little tono impacton theconditionorsurvivalof theindividualHowever theremaybeanonlinear relationship involvingathresholdeffectofmites(Galvaacutenetal2008Haribaletal2005)where only individualswith the absolute greatest number ofmitesarenegativelyimpactedThepossibilityofanonlinearrelationshipbe-tweenmiteabundanceandfitnessmakesthesurvivalresultsinvolvingS ceruleaofpotentialcontinuedinvestigationDespitealackofstatis-ticalsignificanceourpowertodetectatrendwassomewhatlowasonlyasmallproportionofbirdsreturnedtothestudyarea(n=3)OfthesethreeindividualsthatreturnedtwoofthemharboredthetwolowestmiteabundancesofallS ceruleawhilesixS ceruleawiththegreatestabundancesdidnotreturn Inthefutureevaluatingpoten-tialcausativeeffectsthatfeathermiteshaveonhostswouldbestbeexploredexperimentallybydecreasingthenumberofmitesonsomeindividuals (byremoval)andcomparingreproductionandsurvival tocontrolgroups Itwouldbedifficult toexperimentally increasemiteabundancesonindividualsbutthiswouldhypotheticallybeidealtoalsoincludeinanexperimentaldesignAnotherlimitationofourstudyin this regard is thatonly feathermiteswereconsideredexamining(and controlling for) the full symbiont communityonhosts (such asnestmiteswingandbody liceandevenendoparasites)wouldhelpustobetterunderstandhowhostbodyconditionandfitnesscanbeinfluencedbymultiplesymbiontsinteractingonhosts

Although not directly related to our hypotheses differences inmiteabundancebetweenfeathertractsaretoourknowledgeuniqueandpotentiallyhaveimplicationsforfutureresearchonfeathermitesymbioses Previous studies that haveestimatedbothwing and tailfeathermiteabundancehavenotfoundmajordifferencesbetweenthetracts (Papetal2005Stefanetal2015)andBehnkeetal (1999)suggestedthattailfeathermitesaretrivialwhenquantifyingfeathermiteabundancesHoweverinthepresentstudywefoundthatmiteabundanceonrectriceswasgreaterthanonprimariesforbothspecies(despitepossessingmoreprimaryfeathers)andbecausethedifference

betweenthetractswasevengreaterforS ceruleadrovemuchofthevariation inmite abundancebetween species (seeFigure3ab)Thispatternissomewhatsurprisingasrectrices(intheseandmostotherpasserines) are dropped much more readily than primary feathers(TJBpersonalobservation)whichifremainingonarapidlydroppedfeatherwouldlikelycausemortalityofmitesHowevergreatermiteabundanceonrectricesinthesespeciescouldberelatedtoanumberofproximateorultimatefactors

Proximately rectricesmay provide a greater abundance of re-sources(uropygialoil)forfeathermitesifbirdspreferentiallypreenthesefeathersandtailfeathersmayalsoexperiencelessturbulencethanwingfeathersprovidingmoreprotectionforfeathermitesashasbeensuggestedforfeatherlice(Roacutezsa1993)Itisalsopossiblethatultimatelybecausefeathermitespeciesmaydifferbyfeathertract(Fernaacutendez-GonzaacutelezPeacuterez-RodriacuteguezdelaHeraProctorampPeacuterez-Tris2015)abundancesdifferduetodifferentialreproductiveratesor intraspecificcompetition(eg idealdespoticvs idealfreedistribution)Howeverthisisnotlikelyinourcasebecauseforeachof these host species feather mites from the wing and rectriceswereof thesame (host-specific)species in thegenusAmerodectes (Matthews etal in press) No matter the proximate or ultimatecausefordifferentialabundancesourdatasuggestthatmiteabun-dancesobtainedfromrectricescaninfactbeinformativeandbe-cause quantification of tail mite abundance does not require anymajorextensiontofieldmethodsoutlinedherewerecommendthatrectricesbeincludedinfuturestudiesoffeathermitesonlivebirds

InconclusionwefoundthatS cerulea(acanopydwellingopen-cup nesting species) harbored greater abundances of mites thanP citrea (an understory dwelling cavity nester) particularly so ontherectricesThiscontradictsourspecificpredictionbutsupportsour general hypothesis that feather mite abundance differs be-tweenthesetwoecologicallydisparatespeciesSecondlyourdataoverallsupportacommensalsymbiosisbetweenfeathermitesandbothof thesehost speciesTo further improveourunderstandingofthesehighlyspecializedsymbioticsystemsfuturestudiesshould

TABLE 2emspCandidatemodelsdescribingtherelationshipbetweenmiteabundance(linearandquadratic)anddailynestsurvivalbyhostspecies(Setophaga ceruleaandProtonotaria citreafromprimaryfieldsites)andsex(maleandfemale)ForS ceruleathenullmodelincludedageofparentForP citreamalesandfemalesthenullmodelincludednesttype(naturalorartificial)presenceofbroodparasitismageofparentandgeolocatorstatus(ifageolocatorhadbeendeployedpriortothecompletionofthenest)ThedifferencebetweenthemodelwiththelowestAkaikeinformationcriterioncorrectedforsmallsamplesize(AICc)andeachadditionalmodelisgiven(∆AICc)Theweightofevidenceinfavorofamodel(wi)andthenumberofparametersinthemodel(k)arealsogiven

Setophaga cerulea males Protonotaria citrea males Protonotaria citrea females

β plusmn SE ∆AICc wi k β plusmn SE ∆AICc wi k β plusmn SE ∆AICc wi k

Null ndash 006 042 2 ndash 040 035 5 ndash 000a 064 5

Null+mite

00008plusmn0002 204 015 3 0002plusmn0002 000b 042 6 00002plusmn0001 199 024 6

Null+mite+mite2

minus00001plusmn000 000c 043 4 0000004plusmn 0000004

012 023 7 minus0000006plusmn 0000006

324 013 7

aAICc=12917bAICc=9383cAICc = 2015


aimtoevaluatemiteabundance(andtherelationshiptofitness)onadditionalhost speciesofvaryingecological affinities across theirgeographicdistributionsand incorporateexperimentaltestsbyre-movingmitesfromhosts

ACKNOWLEDGMENTS

This research was funded and supported by Arkansas StateUniversityDepartmentofBiologicalSciencesArkansasGameandFishCommission ArkansasAudubon Society Trust PennsylvaniaGame Commission Indiana University of Pennsylvania USDepartmentofAgricultureForestServiceandUSDepartmentofthe Interior Fish andWildlife ServiceWe thank NE Boves andLC Bryant for assistance collecting dataWe thank four anony-mous reviewers for helpful comments on earlier versions of thismanuscript

CONFLICT OF INTEREST

Nonedeclared

AUTHOR CONTRIBUTIONS

AEM and TJB conceived the initial project ideas and designedmethodologyAEMTJBJLLandSHSsecuredfundingfortheprojectAEMTJBDWRMCSandSHScollectedthedataAEManalyzedthedatawithinputfromTJBAEMandTJBledthewritingofthemanuscriptAllauthorscontributedtoeditingandrevisingthemanuscriptandgavefinalapprovalforpublication

ORCID

Alix E Matthews httporcidorg0000-0002-7004-3685

Morgan C Slevin httporcidorg0000-0001-9463-3519

Scott H Stoleson httporcidorg0000-0002-5763-9126

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Behnke J McGregor P Cameron J Hartley I R Shepherd MGilbertFhellipWilesR (1999)Semi-quantitativeassessmentofwingfeather mite (Acarina) infestations on passerine birds from Portugal- evaluation of the criteria for accurate quantification of mite bur-dens The Zoological Society of London 248 337ndash347 httpsdoiorg101111j1469-79981999tb01033x

Blanco G amp Friacuteas O (2001) Symbiotic feather mites synchro-nize dispersal and population growth with host sociality andmigratory disposition Ecography 24 113ndash120 httpsdoiorg101034j1600-05872001240201x

BlancoGTellaJLampPottiJ(1997)Feathermitesongroup-livingred-billedchoughsAnon-parasiticinteractionJournal of Avian Biology28197ndash206httpsdoiorg1023073676970

BovesTJBuehlerDAWoodPBRodewaldADLarkinJLKeyserPDampWigleyTB(2014)Multipleplumagetraitsconveyinformationaboutageandwithin-age-classqualitiesofacanopy-dwellingsongbird

the ceruleanwarblerThe Auk131 20ndash31 httpsdoiorg101642AUK-13-1911

BovesTJFairhurstGDRushingCSampBuehlerDA(2016)Feathercorticosterone levels are related to age and future body conditionbut not to subsequent fitness in a declining migratory songbirdConservation Physiology4cow041httpsdoiorg101093conphyscow041

Buehler D A Hamel P B amp Boves T J (2013) Cerulean Warbler(Setophaga cerulea) The Birds of North America Online httpsdoiorg102173bna511

Carleton R E amp Proctor H C (2010) Feather mites associ-ated with eastern bluebirds (Sialia sialis L) in Georgia includ-ing the description of a new species of Trouessartia (AnalgoideaTrouessartiidae) Southeastern Naturalist 9 605ndash623 httpsdoiorg1016560580090317

ChamberlainSABronsteinJLampRudgersJA(2014)Howcontextde-pendentarespeciesinteractionsEcology Letters17881ndash890httpsdoiorg101111ele12279

DabertJampMironovSV (1999)Originandevolutionoffeathermites(Astigmata)Experimental and Applied Acarology23437ndash454httpsdoiorg101023A1006180705101

DavisAKampCorneliusE (2013)Do infections lead tohigher feathermite loads inbirdsA testwithMycoplasmal conjunctivitis inhousefinches (Haemorhous mexicanus) The Auk130 708ndash714 httpsdoiorg101525auk201313055

Diaz-RealJSerranoDPeacuterez-TrisJFernaacutendez-GonzaacutelezSBermejoACallejaJAhellipJovaniR(2014)Repeatabilityoffeathermiteprev-alenceandintensityinpasserinebirdsPLoS ONE9e107341httpsdoiorg101371journalpone0107341

DinsmoreSJWhiteGCampKnopfFL(2002)AdvancedtechniquesformodelingaviannestsurvivalEcology833476ndash3488httpsdoiorg1018900012-9658(2002)083[3476ATFMAN]20CO2

DontildeaJ Potti J de laHera I BlancoG FriacuteasOampJovani R (2017)Vertical transmission in feathermites Insights into its adaptivevalueEcological Entomology42492ndash499httpsdoiorg101111een12408

Dowling D Richardson D amp Komdeur J (2001) No effects of afeather mite on body condition survivorship or grooming behav-ior in the Seychelles warbler Acrocephalus sechellensis Behavioral Ecology and Sociobiology 50 257ndash262 httpsdoiorg101007s002650100360

DubiecAGoacuteźdźIampMazgajskiTD(2013)GreenplantmaterialinaviannestsAvian Biology Research6133ndash146httpsdoiorg103184175815513X13615363233558

DubininVB(1951)Feathermites(Analgesoidea)PartIIntroductiontothestudyFauna of the USSR Arachnida61ndash363

Fernaacutendez-GonzaacutelezSPeacuterez-RodriacuteguezAdelaHeraIProctorHCampPeacuterez-TrisJ(2015)Differentspacepreferencesandwithin-hostcom-petition promote niche partitioning between symbiotic feathermitespeciesInternational Journal for Parasitology45655ndash662httpsdoiorg101016jijpara201504003

Galvaacuten IAguilera EAtieacutenzar F Barba E Blanco G Cantoacute J L hellipJovaniR(2012)Feathermites(AcariAstigmata)andbodyconditionoftheiravianhostsAlargecorrelativestudyJournal of Avian Biology43273ndash279httpsdoiorg101111j1600-048X201205686x

Galvaacuten IBarbaEPiculoRCantoacuteJLCorteacutesVMonroacutesJShellipProctorHC (2008) Feathermites and birdsAn interactionme-diated by uropygial gland size Journal of Evolutionary Biology 21133ndash144httpsdoiorg101111j1420-9101200701459x

GalvaacutenIampSanzJJ(2006)Feathermiteabundanceincreaseswithuro-pygialglandsizeandplumageyellownessingreattitsParus major Ibis148687ndash697httpsdoiorg101111j1474-919X200600576x

Gaud J amp Atyeo W T (1996) Feather mites of the world (AcarinaAstigmata)ThesupraspecifictaxaPart2illustrationsoffeathermitetaxaAnnales du Musee Royal de LrsquoAfriqie Central Sciences Zoologiques2771ndash436


Hamstra T L amp Badyaev A V (2009) Comprehensive investiga-tion of ectoparasite community and abundance across life historystages of avian host Journal of Zoology 278 91ndash99 httpsdoiorg101111j1469-7998200800547x

HaribalMDhondtAARosaneDampRodriguezE (2005)ChemistryofpreenglandsecretionsofpasserinesDifferentpathways tosamegoal Why Chemoecology 15 251ndash260 httpsdoiorg101007s00049-005-0318-4

Henson S M Galusha J G Hayward J L amp Cushing J M (2007)Modeling territory attendance and preening behavior in a seabirdcolonyas functionsofenvironmental conditions Journal of Biological Dynamics195ndash107httpsdoiorg10108017513750601032679

Johnson N C Graham J H amp Smith F A (1997) Functioningof mycorrhizal associations along the mutualism-parasitismcontinuum The New Phytologist 135 575ndash586 httpsdoiorg101046j1469-8137199700729x

KahleDampWickhamH(2013)ggmapSpatialvisualizationwithggplot2The R Journal5144ndash161

LeungTampPoulinR (2008)ParasitismcommensalismandmutualismExploringthemanyshadesofsymbiosesVie et Milieu58107ndash115

LindstroumlmKMDolnikOYabsleyMHellgrenOOrsquoConnorBPaumlrnH amp Foufopoulos J (2009) Feather mites and internal parasitesin small ground finches (Geospiza fuliginosa Emberizidae) from theGalapagos Islands (Equador) The Journal of Parasitology 95 39ndash45httpsdoiorg101645GE-16551

Lovette IJPeacuterez-EmaacutenJ L SullivanJPBanksRCFiorentino ICoacuterdoba-CoacuterdobaShellipBerminghamE(2010)Acomprehensivemul-tilocusphylogenyforthewood-warblersandarevisedclassificationofthe Parulidae (Aves)Molecular Phylogenetics and Evolution57 753ndash770httpsdoiorg101016jympev201007018

MatthewsA E Klimov P B ProctorH CDowlingA P GDienerLHager SBhellipBovesTJ (inpress)Cophylogenetic assessmentofNewWorldwarblers (Parulidae)and their symbiotic feathermites(Proctophyllodidae)Journal of Avian Biologyhttpsdoiorg101111jav01580

McKim-LouderMIHooverJPBensonTJampSchelskyWM(2013)Juvenile survival in a neotropical migratory songbird is lower thanexpected PLoS ONE 8 e56059 httpsdoiorg101371journalpone0056059

MeleacutendezLLaioloPMironovSGarciacuteaMMagantildeaOampJovaniR(2014) Climate-driven variation in the intensity of a host-symbiontanimal interaction along a broad elevation gradient PLoS ONE 9e101942httpsdoiorg101371journalpone0101942

MoyerBRDrownDMampClaytonDH(2002)LowhumidityreducesectoparasitepressureImplicationsforhostlifehistoryevolutionOikos97223ndash228httpsdoiorg101034j1600-07062002970208x

Pap P LToumlkoumllyi J amp SzeacutepT (2005)Hostndashsymbiont relationship andabundanceoffeathermitesinrelationtoageandbodyconditionofthebarnswallow(Hirundo rustica)AnexperimentalstudyCanadian Journal of Zoology831059ndash1066httpsdoiorg101139z05-100

Pap P L Vaacutegaacutesi C I Osvaacuteth G Muresan C amp Barta Z (2010)Seasonality in the uropygial gland size and feather mite abun-dance in house sparrows Passer domesticus Natural covariation andan experiment Journal of Avian Biology 41 653ndash661 httpsdoiorg101111j1600-048X201005146x

PetitLJ (1999)ProthonotaryWarbler (Protonotaria citrea) The Birds of North America Onlinehttpsdoiorg102173bna408

ProctorHC(2003)Feathermites(AcariAstigmata)EcologybehaviorandevolutionAnnual Review of Entomology48185ndash209httpsdoiorg101146annurevento48091801112725

PyleP(1999)Identification Guide to North American Birds A Compendium of Information on Identifying Ageing and Sexing ldquonear-Passerinesrdquo and Passerines in the HandBolinasCaliforniaSlateCreekPress

RCoreTeam(2016)R A language and environment for statistical computing ViennaAustriaRCoreTeamURLhttpwwwr-projectorg

RoacutezsaL(1993)Anexperimentaltestofthesitespecificityofpreeningtocontrol lice inferalpigeonsThe Journal of Parasitology79968ndash970httpsdoiorg1023073283742

Schulte-HosteddeA I Zinner BMillar J S ampHickling G J (2005)Restitution ofmass-size residualsValidating body condition indicesEcology86155ndash163httpsdoiorg10189004-0232

SolerJJPeralta-SaacutenchezJMMartiacuten-PlateroAMMartiacuten-VivaldiMMartiacutenez-BuenoMampMoslashllerAP (2012)Theevolutionof sizeoftheuropygialglandMutualisticfeathermitesanduropygialsecretionreducebacterial loadsofeggshellsandhatchingfailuresofEuropeanbirds Journal of Evolutionary Biology 25 1779ndash1791 httpsdoiorg101111j1420-9101201202561x

StefanLMGoacutemez-DiacuteazEElgueroEProctorHCMcCoyKDampGonzaacutelez-SoliacutesJ (2015)NichepartitioningoffeathermiteswithinaseabirdhostCalonectris Borealis PLoS ONE10e0144728httpsdoiorg101371journalpone0144728

ThompsonJNampCunninghamBM(2002)GeographicstructureanddynamicsofcoevolutionaryselectionNature417735ndash738httpsdoiorg101038nature00810

Tonra C M Hallworth M T Boves T J Bulluck L P Johnson MViveretteChellipJohnsonEI(inreview)WeakmigratoryconnectivitydespitemigratorydivideImplicationsfornonbreedingconservationofawetlandsongbirdBiological Conservation

VillaSMLeBohecCKoopJAHProctorHCampClaytonDH(2013) Diversity of feather mites (Acari Astigmata) on Darwinrsquosfinches The Journal of Parasitology 99 756ndash762 httpsdoiorg10164512-1121

WhiteGCampBurnhamKP (1999)ProgramMARKSurvivalestima-tionfrompopulationsofmarkedanimalsBird Study46S120ndashS139httpsdoiorg10108000063659909477239

WickhamH(2009)ggplot2 Elegant Graphics for Data AnalysisNewYorkSpringer-Verlaghttpsdoiorg101007978-0-387-98141-3

WilesRCameronJBehnkeJMHartleyIRGilbertFSampMcGregorPK(2000)WingfeathermiteinfestationsonpasserinebirdsSeasonandambientairtemperatureinfluencethedistributionofProctophyllodes styliferacrossthewingsofbluetits(Parus caeruleus) Canadian Journal of Zoology781397ndash1407httpsdoiorg101139z00-068

How to cite this articleMatthewsAELarkinJLRaybuckDWSlevinMCStolesonSHBovesTJFeathermiteabundancevariesbutsymbioticnatureofmite-hostrelationshipdoesnotdifferbetweentwoecologicallydissimilarwarblersEcol Evol 201881227ndash1238 httpsdoiorg101002ece33738


(LeungampPoulin2008)Birdsharboravarietyofectosymbiontsincludingfeathermites(AstigmataAnalgoideaPterolichoidea)whosesymbioticrelationshipwith theiravianhostshas recentlybeendebated (Galvaacutenetal20082012Soleretal2012)Feathermitesareobligatoryec-tosymbioticarthropodsthat inhabitthesmallspacesbetweenfeatherbarbsandarethoughttoprimarilyfeedonoilysecretionsfromtheuro-pygialglandwhicharedistributedacrossfeathersbypreening(Proctor2003)Feathermiteshavestreamlinedbodiesandspecializedambulacra(feet) thatallowthemtohold tightlyonto featherbarbulesandresistturbulentairflowduringflight(DabertampMironov1999)

Thespecializeddietaryandmorphologicaladaptationsoffeathermites suggest the strong symbiotic relationship betweenmites andtheir avian hosts However the specific nature of this relationship(positive negative or neutral) and any context dependency of thesymbiosis has not been resolved Thus few generalizations can bemadeaboutfactorsthatdrivevariationinthisrelationshipbothwithinandamongspecies

Mostpreviousworkexploringthisrelationshiphastestedforcor-relationsbetweenmiteabundanceandcurrentphysiologicalconditionForexamplecorrelationsbetweenfeathermiteabundanceandhostbodymassandotherbodyconditionindiceshaveledtoinferencesofbothmutualism(BlancoampFriacuteas2001Lindstroumlmetal2009VillaLeBohecKoopProctorampClayton2013)andcommensalism (BlancoTella amp Potti 1997 Carleton amp Proctor 2010 Davis amp Cornelius2013)Furthermorepreviousstudiestypicallyhaveconcentratedonhowmiteabundancecaninfluenceasinglecomponentofhostcurrentfitness(DowlingRichardsonampKomdeur2001GalvaacutenampSanz2006Galvaacutenetal2012)limitingtheconclusionsthatcanbedrawnaboutthenatureofthesymbiosisThisisalsolimitingbecausealageffectofmitesispossibleandfewstudieshavetakenthenextsteptorelatemiteabundancetofuturehostfitness(reproductiveperformanceandorannualsurvival)whichmaydemonstratehowmitesaffectanindi-vidualoveritslifetimeInfacttoourknowledgeonlyonestudy(PapToumlkoumllyiampSzeacutep2005)hasassessedhowfeathermiteabundancere-latesbothtoreproductiveparametersandannualsurvivaltheyfoundnorelationshipsineithercase

Theseindividualcasesalsohighlightamajorvoidinourunderstand-ingofrelationshipsbetweenfeathermitesandtheirhostsAlthoughanumberofstudieshaveexploredthepotentialfactorsthatarerelatedtovariation inabundanceoffeathermitesonhostswithinaspeciesfew studies have then assessed how those same factors contributetocontextdependencyoftheeffectsoffeathermitesonhostfitnessamongandwithinspeciesAvarietyofamong- (egecologicalaffili-ations)andwithin-speciesfactors (egageorsex)mayberelatedtomiteabundanceandsomemaytheninteractwithmiteabundancetoinfluencehost fitnessAmongspecies somehostsmayhavegreatermite abundances because of their ecological context or life historystrategy(Diaz-Realetal2014Galvaacutenetal2008)whichinturncaninfluencehowmitescanaffectindividualhostfitnessThismaybees-peciallytrueifthereisathresholdatwhichhostingmitesbecomesbur-densome(Galvaacutenetal2008HaribalDhondtRosaneampRodriguez2005)Alternativelyindividualsofsomespeciesmaybeabletosustainanequivalentmiteabundancewithnoeffectsonfitness

Forexample a speciesrsquo nestingecologymay influencebothmiteabundanceandtheeffectsofmitesonhost fitnessas feathermitesaredependentuponthemicroclimateofthehost(andultimatelythehostrsquosenvironment)During thebreedingseasonmuchof thehostrsquosenvironmentisatthenestespeciallyforfemalesInadditionitisatthenestwherefeathermitesprimarilydispersetonewhosts(theoffspringDontildeaetal2017)whichmeansthattheywouldbeevenmoreaffectedbythenestenvironmentastheymovefromhosttohostSpecificallyunderstory dwelling cavity-nesting species may occupy nests thatmakethemmoresusceptibletoparasiticmiteabundancesthantheircanopydwellingopen-cupnestingcounterparts(GalvaacutenampSanz2006)ThisismechanisticallypossibleforseveralreasonsFirstabioticcondi-tionssuchastemperatureandhumiditywithincavitiesintheunder-storymaybemoresuitableformitesandthushostsmayhavegreatermiteabundances(atleastduringthebreedingseason)Thisisbecausethegreatestabundanceofmitesonindividualsoccursatrelativelyhightemperatures(above20degCWilesetal2000)andmanyectosymbiontsincreaseinabundanceasrelativehumidityincreases(MoyerDrownampClayton2002)Furthermoresecondarycavity-nestingspecies(thosethatnest incavitiesthathavebeenmadebyheterospecifics)maybeevenmoresusceptibletoparasiticmiteabundancesbecauseofthepo-tentialformitestoliveinpreviouslyusedcavitiesandtransfertonewhostsapossibilitythathasbeenproposedbutnotyettested(CarletonampProctor2010)Finallyspecieswiththislifehistorystrategy(second-arycavity-nesting)couldalsoincreasetheprobabilityofaforeignmitespeciesbeinghorizontallytransmittedtoanevolutionarilynaiumlvehostandtheresultingincipientspecies-interactionmayfallfurtherontheparasiticsideofthesymbioticcontinuum(JohnsonGrahamampSmith1997LeungampPoulin2008)

Justasinterspecificvariationinecologymayberelatedtoboththeabundanceoffeathermitesandtheireffectsonhostfitnessintraspe-cifictraits(egsexandage)mayalsobeimportantAlthoughvariationinmiteabundancebyhostsexhasbeeninvestigatedbefore(CarletonampProctor2010HamstraampBadyaev2009)noobviouspatternshaveemergedandthereiscurrentlynoclearexplanationastowhythisvari-ationmayexistHere again a speciesrsquo ecological contextmayplay aroleForexampleinspeciesthatexhibittypicalsexrolesfemalesmayharborgreatermiteabundancesthantheirmalepartnersbecausetheyspendmoretimeonthenestlayingandincubatingeggsandbroodingtheiryoungTheymayalsobemorenegativelyaffectedbymiteses-pecially iftheyharbormiteabundancesabovesomethresholdduringthebreedingseasonAgemayalsobeafactorbutthereareconflict-ingpatterns inthe literatureForexample inBarnSwallows (Hirundo rustica)adultshadhigherfeathermiteabundancesthanjuveniles(Papetal2005)Thisresultcanbejustifiedbecausemitestypicallymatureoneeggatatime(Dubinin1951)anditmaytaketimeformitepopula-tionstobuilduponyoungbirdsHoweverDavisandCornelius(2013)foundtheoppositepatternwithyoungerHouseFinches(Haemorhous mexicanus)harboringmoremitesthanadultsInadditionitisunknownhowtheinteractionbetweenecologicalaffiliationageandsexmayin-fluencefeathermiteabundanceorfeathermiteimpactsonhostfitness

In this study we explored how feather mite abundance variedamongspecies(dueinparttodifferingnestingecologies)andwithin








































3emsp |emspRESULTS



















etop

haga

cer

uleaandP

roto

nota

ria c




Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Bodycondition(L)

Totalmites

lt0001plusmnlt0001

t = 0

38

117

1lt0001plusmnlt0001

t = 0

44

3866


t=minus074

4446

Julian

001plusmn0008

t=206

1106

lt0001plusmnlt0001

t=006

3895

minus0006plusmn0007

t=minus083

444

1

Age

023plusmn015

t=156

111


t=minus030

3876

minus012plusmn026

t=minus046

4465

Bodycondition(Q)

Totalmites


t=minus097

1036

0001plusmnlt0001

t = 1

34

3719

lt0001plusmnlt0001

t=064

435

2

Totalmites2

lt0001plusmnlt0001

t = 1

11

1029

lt0001plusmnlt0001

t=minus127

372


t=minus096

433

4

Julian

001plusmnlt0001

t = 2

17

1006

lt0001plusmn0004

t=009

3792

minus0006plusmn0007

t=minus089

433

8

Age

015plusmn016

t=097

103

5minus0004plusmn020

t=minus002

3798

minus015plusmn027

t=minus056

435

8

Offspringfledged(L)

Totalmites


Z=minus029

37

7lt0001plusmnlt0001

Z=129

2919


Z=minus186

4306

Nesttype

mdashmdash

mdashmdash

minus006plusmn021

Z=minus033

297

4006plusmn016

Z =

042

4367

Age

minus099plusmn068

Z=minus147

31

4059plusmn023

Z=260

290

09015plusmn017

Z=092

4336

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2999

minus215plusmn059

Z=minus37

43lt

001

Geolocator

status

mdashmdash

mdashmdash

017plusmn032

Z =

055

295

8018plusmn022

Z =

083

434

1

Offspringfledged(Q)

Totalmites

0009plusmn0007

Z=146

21

4lt0001plusmn0001

Z =

004

2897

lt0001plusmnlt0001

Z=094

423

5

Totalmites2


Z=minus159

21

1lt0001plusmnlt0001

Z=046

2864


Z=minus160

421

1

Nesttype

mdashmdash

mdashmdash

minus009plusmn022

Z=minus045

2865

007plusmn022

Z =

047

4264

Age

minus0002plusmn0008

Z=minus031

27

5057plusmn023

Z=246

280

1015plusmn017

Z=092

4236

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2899

minus22plusmn059

Z=minus367

42lt

001

Geolocator

status

mdashmdash

mdashmdash

019plusmn032

Z=061

285

4007plusmn016

Z =

080

424

2

Survival(L)

Totalmites

minus0003plusmn0002

Z=minus148

141

40002plusmn0002

Z=096

383

4lt0001plusmn0002

Z=minus002

4598

(Continues)







Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

384

2192plusmn099

Z=194

450

5

Age

minus082plusmn167

Z=minus049

1463

141plusmn094

Z=149

381

4189plusmn075

Z =

253

450

1

Survival(Q)

Totalmites

minus0009plusmn0007

Z=minus126

132

1lt0001plusmn0006

Z =

018

378

5lt0001plusmn0006

Z=016

448

7

Totalmites2

lt0001plusmnlt0001

Z=092

1336


Z=019

378


Z=minus018

4486

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

374

2192plusmn099

Z=194

440

5

Age

minus176plusmn228

Z=minus077

134

4137plusmn097

Z =

037

3716

188plusmn075

Z=249

440

1












Null+mite


Null+mite+mite2


012 023 7 minus0000006plusmn 0000006

324 013 7




ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES





























































































3emsp |emspRESULTS



















etop

haga

cer

uleaandP

roto

nota

ria c




Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Bodycondition(L)

Totalmites

lt0001plusmnlt0001

t = 0

38

117

1lt0001plusmnlt0001

t = 0

44

3866


t=minus074

4446

Julian

001plusmn0008

t=206

1106

lt0001plusmnlt0001

t=006

3895

minus0006plusmn0007

t=minus083

444

1

Age

023plusmn015

t=156

111


t=minus030

3876

minus012plusmn026

t=minus046

4465

Bodycondition(Q)

Totalmites


t=minus097

1036

0001plusmnlt0001

t = 1

34

3719

lt0001plusmnlt0001

t=064

435

2

Totalmites2

lt0001plusmnlt0001

t = 1

11

1029

lt0001plusmnlt0001

t=minus127

372


t=minus096

433

4

Julian

001plusmnlt0001

t = 2

17

1006

lt0001plusmn0004

t=009

3792

minus0006plusmn0007

t=minus089

433

8

Age

015plusmn016

t=097

103

5minus0004plusmn020

t=minus002

3798

minus015plusmn027

t=minus056

435

8

Offspringfledged(L)

Totalmites


Z=minus029

37

7lt0001plusmnlt0001

Z=129

2919


Z=minus186

4306

Nesttype

mdashmdash

mdashmdash

minus006plusmn021

Z=minus033

297

4006plusmn016

Z =

042

4367

Age

minus099plusmn068

Z=minus147

31

4059plusmn023

Z=260

290

09015plusmn017

Z=092

4336

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2999

minus215plusmn059

Z=minus37

43lt

001

Geolocator

status

mdashmdash

mdashmdash

017plusmn032

Z =

055

295

8018plusmn022

Z =

083

434

1

Offspringfledged(Q)

Totalmites

0009plusmn0007

Z=146

21

4lt0001plusmn0001

Z =

004

2897

lt0001plusmnlt0001

Z=094

423

5

Totalmites2


Z=minus159

21

1lt0001plusmnlt0001

Z=046

2864


Z=minus160

421

1

Nesttype

mdashmdash

mdashmdash

minus009plusmn022

Z=minus045

2865

007plusmn022

Z =

047

4264

Age

minus0002plusmn0008

Z=minus031

27

5057plusmn023

Z=246

280

1015plusmn017

Z=092

4236

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2899

minus22plusmn059

Z=minus367

42lt

001

Geolocator

status

mdashmdash

mdashmdash

019plusmn032

Z=061

285

4007plusmn016

Z =

080

424

2

Survival(L)

Totalmites

minus0003plusmn0002

Z=minus148

141

40002plusmn0002

Z=096

383

4lt0001plusmn0002

Z=minus002

4598

(Continues)







Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

384

2192plusmn099

Z=194

450

5

Age

minus082plusmn167

Z=minus049

1463

141plusmn094

Z=149

381

4189plusmn075

Z =

253

450

1

Survival(Q)

Totalmites

minus0009plusmn0007

Z=minus126

132

1lt0001plusmn0006

Z =

018

378

5lt0001plusmn0006

Z=016

448

7

Totalmites2

lt0001plusmnlt0001

Z=092

1336


Z=019

378


Z=minus018

4486

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

374

2192plusmn099

Z=194

440

5

Age

minus176plusmn228

Z=minus077

134

4137plusmn097

Z =

037

3716

188plusmn075

Z=249

440

1












Null+mite


Null+mite+mite2


012 023 7 minus0000006plusmn 0000006

324 013 7




ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES
































































etop

haga

cer

uleaandP

roto

nota

ria c




Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Bodycondition(L)

Totalmites

lt0001plusmnlt0001

t = 0

38

117

1lt0001plusmnlt0001

t = 0

44

3866


t=minus074

4446

Julian

001plusmn0008

t=206

1106

lt0001plusmnlt0001

t=006

3895

minus0006plusmn0007

t=minus083

444

1

Age

023plusmn015

t=156

111


t=minus030

3876

minus012plusmn026

t=minus046

4465

Bodycondition(Q)

Totalmites


t=minus097

1036

0001plusmnlt0001

t = 1

34

3719

lt0001plusmnlt0001

t=064

435

2

Totalmites2

lt0001plusmnlt0001

t = 1

11

1029

lt0001plusmnlt0001

t=minus127

372


t=minus096

433

4

Julian

001plusmnlt0001

t = 2

17

1006

lt0001plusmn0004

t=009

3792

minus0006plusmn0007

t=minus089

433

8

Age

015plusmn016

t=097

103

5minus0004plusmn020

t=minus002

3798

minus015plusmn027

t=minus056

435

8

Offspringfledged(L)

Totalmites


Z=minus029

37

7lt0001plusmnlt0001

Z=129

2919


Z=minus186

4306

Nesttype

mdashmdash

mdashmdash

minus006plusmn021

Z=minus033

297

4006plusmn016

Z =

042

4367

Age

minus099plusmn068

Z=minus147

31

4059plusmn023

Z=260

290

09015plusmn017

Z=092

4336

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2999

minus215plusmn059

Z=minus37

43lt

001

Geolocator

status

mdashmdash

mdashmdash

017plusmn032

Z =

055

295

8018plusmn022

Z =

083

434

1

Offspringfledged(Q)

Totalmites

0009plusmn0007

Z=146

21

4lt0001plusmn0001

Z =

004

2897

lt0001plusmnlt0001

Z=094

423

5

Totalmites2


Z=minus159

21

1lt0001plusmnlt0001

Z=046

2864


Z=minus160

421

1

Nesttype

mdashmdash

mdashmdash

minus009plusmn022

Z=minus045

2865

007plusmn022

Z =

047

4264

Age

minus0002plusmn0008

Z=minus031

27

5057plusmn023

Z=246

280

1015plusmn017

Z=092

4236

Brood

parasitism

mdashmdash

mdashmdash

minus172plusmn1484

Z=minus001

2899

minus22plusmn059

Z=minus367

42lt

001

Geolocator

status

mdashmdash

mdashmdash

019plusmn032

Z=061

285

4007plusmn016

Z =

080

424

2

Survival(L)

Totalmites

minus0003plusmn0002

Z=minus148

141

40002plusmn0002

Z=096

383

4lt0001plusmn0002

Z=minus002

4598

(Continues)







Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

384

2192plusmn099

Z=194

450

5

Age

minus082plusmn167

Z=minus049

1463

141plusmn094

Z=149

381

4189plusmn075

Z =

253

450

1

Survival(Q)

Totalmites

minus0009plusmn0007

Z=minus126

132

1lt0001plusmn0006

Z =

018

378

5lt0001plusmn0006

Z=016

448

7

Totalmites2

lt0001plusmnlt0001

Z=092

1336


Z=019

378


Z=minus018

4486

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

374

2192plusmn099

Z=194

440

5

Age

minus176plusmn228

Z=minus077

134

4137plusmn097

Z =

037

3716

188plusmn075

Z=249

440

1












Null+mite


Null+mite+mite2


012 023 7 minus0000006plusmn 0000006

324 013 7




ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES




























































Seto

phag

a ce

rule

a m

ales

Prot

onot

aria

citr

ea m

ales

Prot

onot

aria

citr

ea fe

mal

es

β plusmn

SETe

st S

tatis

ticdf

pβ

plusmn SE

Test

Sta

tistic

dfp

β plusmn

SETe

st

Stat

istic

dfp

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

384

2192plusmn099

Z=194

450

5

Age

minus082plusmn167

Z=minus049

1463

141plusmn094

Z=149

381

4189plusmn075

Z =

253

450

1

Survival(Q)

Totalmites

minus0009plusmn0007

Z=minus126

132

1lt0001plusmn0006

Z =

018

378

5lt0001plusmn0006

Z=016

448

7

Totalmites2

lt0001plusmnlt0001

Z=092

1336


Z=019

378


Z=minus018

4486

Geolocator

status

mdashmdash

mdashmdash

minus079plusmn098

Z=minus081

374

2192plusmn099

Z=194

440

5

Age

minus176plusmn228

Z=minus077

134

4137plusmn097

Z =

037

3716

188plusmn075

Z=249

440

1












Null+mite


Null+mite+mite2


012 023 7 minus0000006plusmn 0000006

324 013 7




ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES
































































Null+mite


Null+mite+mite2


012 023 7 minus0000006plusmn 0000006

324 013 7




ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES
























































ACKNOWLEDGMENTS



Nonedeclared



ORCID




REFERENCES






















































feather mite abundance varies but symbiotic nature …...feather mites (astigmata: analgoidea,...

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