Feather mite abundance varies but symbiotic nature …...feather mites (Astigmata: Analgoidea, Pterolichoidea),whose symbiotic relationship with their avian hosts has recently been
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Ecology and Evolution 201881227ndash1238 emsp|emsp1227wwwecolevolorg
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
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
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
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)
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
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
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)
emspensp emsp | emsp1231MATTHEWS ET Al
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
F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
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
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)
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
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
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)
emspensp emsp | emsp1231MATTHEWS ET Al
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
F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
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
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
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
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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
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
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
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
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
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)
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
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
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)
emspensp emsp | emsp1231MATTHEWS ET Al
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
F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
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
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)
emspensp emsp | emsp1231MATTHEWS ET Al
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
F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
emspensp emsp | emsp1231MATTHEWS ET Al
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
F IGURE 2emspProcedureforobjectivelyquantifyingfeathermiteabundanceonfeathersThefeathers(eitherprimariesorrectrices)areoutstretchedheldagainstanambientbackgroundandcovertsarepushedoutoftheway(inordertoseethefulllengthofthefeather)Sometimesmultiplephotosweretakeninordertoseemitesonallnineprimariesoneachwingorall12rectrices(forexamplethreefeathersperphoto)Amacro-lenssettingonadigitalcamerawasusedandclarityofeachphotowascheckedinthefieldNoflashwasusedAclose-upofthefeathermitesbetweenfeatherbarbscanbeseenintheinsetphotograph
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
1232emsp |emsp emspensp MATTHEWS ET Al
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)
32emsp|emspHypothesis 1 Mite abundance differs by (a) species (b) sex and (c) age
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
33emsp|emspHypothesis 2 Relationship between mite abundance and body conditionfitness differs by species and within species sex
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)
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
emspensp emsp | emsp1233MATTHEWS ET Al
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
emspensp emsp | emsp1235MATTHEWS ET Al
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
ltminus0001plusmnlt0001
Z=019
378
4ltminus0001plusmnlt0001
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)
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
1236emsp |emsp emspensp MATTHEWS ET Al
(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
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
emspensp emsp | emsp1237MATTHEWS ET Al
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
REFERENCES
BatesDMaumlchlerMBolkerBampWalkerS(2014)Fittinglinearmixed-effectsmodelsusinglme4Journal of Statistical Software671ndash48
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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
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
1238emsp |emsp emspensp MATTHEWS ET Al
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
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
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
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How to cite this articleMatthewsAELarkinJLRaybuckDWSlevinMCStolesonSHBovesTJFeathermiteabundancevariesbutsymbioticnatureofmite-hostrelationshipdoesnotdifferbetweentwoecologicallydissimilarwarblersEcol Evol 201881227ndash1238 httpsdoiorg101002ece33738