Stable isotope ratios in alpine rock ptarmigan and black grouse sampled along a precipitation gradient

Stable isotope ratios in alpine rock ptarmigan and black grouse sampled along a precipitation gradient

Nina Dehnhard

, Elizabeth Yohannes

, Hannes Jenny

, Gernot Segelbacher

aUniversityofAntwerp,DepartmentBiology–BehaviouralEcology&EcophysiologyGroup,CampusDrieEiken, Universiteitsplein1,2610Antwerp(Wilrijk),Belgium

bUniversityofKonstanz,LimnologicalInstitute,Mainaustrasse252,78457Konstanz,Germany

cDepartmentofWildlifeandFisheryServiceGrison,Loëstrasse14,7001Chur,Switzerland

dWildlifeEcology&Management,UniversityofFreiburg,TennenbacherStr.4,79106Freiburg,Germany

Abstract

Rockptarmigan(Lagopusmuta)andblackgrouse(Tetraotetrix)aretwocloselyrelatedalpinebirdspeciesthatformrelict populationsintheEuropeanAlps.Besidesmanifoldanthropogenicinfluencesinthisregion,globalclimatechangeisforecastto leadtosignificantchangesintemperaturesandprecipitation.Wehereanalysedstableisotoperatios(␦¹³Cand␦¹⁵N)offeathers ofbothbirdspeciesandtheirpotentialdietaryplantsacrossalongitudinalprecipitationgradientinsouth-eastSwitzerland.

Plant␦¹³Cwashigherathigheraltitudesandindrierareas(coincidingwithhigherlongitudes)whileplant␦¹⁵Ndidnotdiffer geographically.Blackgrouse␦¹³Creflectedthelongitudinalpatterninprecipitationandplant␦¹³C,andtherewasnoindication forachangeindietarycompositionwithprecipitation(i.e.nosignificantchangesin␦¹⁵N).Incontrast,rockptarmigan␦¹³Cwas independentofprecipitationandplant␦¹³Cvaluesandshowedasignificantincreasein␦¹⁵Ntowardsdrierareas,suggestinga potentialdietaryshift.

Inrockptarmigan,wefurthermoreinvestigatedintraspecificdifferenceswithage,betweenmalesandfemalesandamong years, anddidnot findany biologically meaningful intraspecificdifferences.Interspecifically, rockptarmiganfeathershad significantlyhigher␦¹³Candlower␦¹⁵Nvaluesthanblackgrouse,reflectingadietarysegregationbetweenbothspecies.This maypartlybeduetothehigheraltitudinaldistributionofrockptarmiganincombinationwithanaltitudinalgradientinplant

␦¹³C.Inaddition,however,speciesalsosegregatedin␦¹⁵N,mostlikelycausedbyahigherproportionofinvertebratedietin blackgrouse.

Zusammenfassung

Alpenschneehuhn(Lagopusmuta)undBirkhuhn(Tetraotetrix)sindzweinaheverwandteVogelarten,dieReliktpopulationen indenEuropäischenAlpenbilden.NebenvielfältigenanthropogenenEinflüssenindieserRegionwerdenwegendesglobalen KlimawandelssignifikanteVeränderungen inTemperaturund Niederschlagerwartet.Wiranalysierten diestabile Isotopen- zusammensetzung(␦¹³Cund␦¹⁵N)vonFedernsowie potentiellenNahrungspflanzenentlangeinesNiederschlagsgradienten imSüdostenderSchweiz.

∗Correspondingauthor.Tel.:+32032652347;fax:+32038202271.

E-mailaddress:nina.dehnhard@uantwerpen.be(N.Dehnhard).

Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-348936

https://dx.doi.org/10.1016/j.baae.2016.04.007

Die␦¹³C-WertederNahrungspflanzennahmenmitTrockenheit(übereinstimmendmitzunehmendenLängengraden)undHöhe zu,währenddieGeographiekeineAuswirkungenaufdie␦¹⁵N-WertederNahrungspflanzenhatte.␦¹³C-WertevonBirkhuhn- federnreflektiertendenlongitudinalenGradienteninNiederschlagundPflanzen-␦¹³C-Werten,undesgabkeineAnzeichenfür eineÄnderungderNahrungszusammensetzungentlangdesNiederschlagsgradienten(d.h.keinesignifikantenVeränderungen in␦¹⁵N).InAlpenschneehuhnfedernhingegenwarendie␦¹³C-WerteunabhängigvonNiederschlagundPflanzen-␦¹³C-Werten.

Die␦¹⁵N-WerteinAlpenschneehuhnfedernnahmenzudemsignifikantmitTrockenheitzu,waspotentiellaufeineVeränderung derNahrungszusammensetzungentlangdesNiederschlagsgradientenhinweist.

An Alpenschneehühnern untersuchten wir auch intraspezifische Unterschiede zwischen Altersklassen, Männchen und Weibchen sowie verschiedenen Jahren, fanden jedoch keine biologisch aussagekräftigen intraspezifischen Unterschiede.

Interspezifischwiesen Alpenschneehuhnfedernsignifikanthöhere␦¹³Cund niedrigere␦¹⁵N-Werteauf alsBirkhühner, was eineAbgrenzungderbeidenArteninihrerNahrung reflektiert.DieskannzumTeildurchdieunterschiedlicheNutzungdes LebensraumsinKombinationmitdemGradienteninPflanzen-␦¹³CmitansteigenderHöheerklärtwerden.Alpenschneehühner erschließenauchhochalpineRegionen,währendBirkhühnernahederBaumgrenzeverbleiben.Zusätzlichunterschiedensich beideArtenjedochauchinihren␦¹⁵N-Werten,wasvermutlichdurcheinenhöherenAnteilvonInvertebrateninderNahrung vonBirkhühnernverursachtwird.

Keywords: EuropeanAlps;Globalclimatechange;Plantisotope;Precipitation;Stableisotopeanalysis

Introduction

Astypicalformountainousareas,theEuropeanAlpsshow ahighdiversityofdifferentclimatezonesonarelativelysmall scale,mainlydrivenbythecontinuoustemperaturedecrease withelevation(Frey&Lösch2004).Inaddition,theEuro- peanAlpsformabarrieragainstweatherfronts,whichleads tohigherprecipitationattheedgesanddrierconditions in thecentralareas(Frey&Lösch2004).Astemperatureand moistureareimportantdeterminantsoftheecologicalniche ofplantsandanimals(Begon,Townsend,&Harper,2006), thisdiversityinAlpineclimatehabitatsisalsoreflected in thediversityofhabitatsandspecies.ThisrichnessinAlpine wildlifeis,however,severelyaffectedbyanthropogenicinflu- ences,such as the use of pasturesand changesin grazing regimes (Meusburger &Alewell 2008; Patthey, Signorell, Rotelli,&Arlettaz,2012;Paschettaetal.,2013),installation ofhydroelectricpowerplants(Truffer,Markard,Bratrich,&

Wehrli,2001;Fette,Weber,Peter,&Wehrli,2007),orrecre- ationalsnowsportactivities(Braunisch,Patthey,&Arlettaz, 2010; Negro, Isaia, Palestrini, Schoenhofer, & Rolando, 2010).Inaddition,theEuropeanAlpsareoneoftheareaswith thestrongestobservedwarmingtrendworldwide,regionally showingincreasesof1–2^◦Cofaverageannualairtempera- tureduringthe20thcentury(Begert,Schlegel,&Kirchhofer, 2005;Parolo &Rossi 2008).Along withfurthertempera- tureincreases,climatemodelsfortheEuropeanAlpspredict changesinprecipitationpatterns,withgenerallydriersum- mers and wetter winters (including rain), andan increase of extreme weather events including extreme rainfalls but alsotemporaldroughts(Zimmermann,Gebetsroither,Züger, Schmatz,&Psomas,2013;Gobietetal.,2014).Theseclima- tologicaleffectswillleadtoanelevationofthetreeline,which ispartlyalreadyvisible(Dullinger,Dirnböck, &Grabherr,

2004).Inadditiontolandusechangeswewilllikelyobserve areductioninsizeofhigh-alpinemeadowhabitatsthatgoes alongwithanoverallbiodiversityloss(Dirnböck,Dullinger,

&Grabherr,2003;Engleretal.,2011).

Manyofthenowthreatenedhigh-altitudespeciesarerelict speciesthathavesurvivedinmountainousareassincethelast glacialperiod,boostinglocalbiodiversity(Ohlemülleretal., 2008; Dirnböck, Essl, & Rabitsch, 2011).Two prominent andcloselyrelatedspeciesthatformrelictpopulationsinthe EuropeanAlpsarerockptarmigan(Lagopusmuta)andblack grouse(Lyrurustetrix).Rockptarmiganarefoundinrocky areasabovethetreeline(fromabout1800manduptomore than3000m)(GlutzvonBlotzheim,Bauer,&Bezzel,1973;

Pernollet, Korner-Nievergelt, & Jenni, 2015). In contrast, blackgrouseshowaborealdistribution,withthemainalpine habitatbeingtheupperforestedge,i.e.theareaofthetree line(GlutzvonBlotzheimetal.1973).Populationsofboth species in the European Alps were considered as stable until the mid-1990s (Schmid, Luder, Naef-Daenzer, Graf,

&Zbinden,1998;Peronace,Cecere, Gustin,&Rondinini, 2012). However, in the following decade rock ptarmigan declinedbyabout30%inbothSwitzerland(Keller,Gerber, Schmid,Volet,&Zbinden,2010)andItaly(Peronaceetal.

2012).In thesameperiod, blackgrousenumbers declined byupto20%inItaly(Peronaceetal.2012).Whetherthese decliningtrendsthat alsopersist onaglobal scale(Storch 2007)arealreadycausedbytheeffectsofclimatechange,or potentiallyotheranthropogenicinfluences,isunknownand analysesareaggravatedbythefactthatpopulationdeclines vary insize amongregions(Furrer et al.2016).However, with ongoingclimate change effects, bothrockptarmigan andblackgrousewillhavetotracktheshiftofthetreeline tohigher elevations,atrendthatis alreadyvisibleinrock ptarmigan(Pernolletetal.2015).Especiallyunderwarming

scenarios exceeding 2^◦C, both species will furthermore sufferfromalossinsuitablehabitat(Revermann,Schmid, Zbinden,Spaar,&Schroder,2012;Zurelletal.,2012).

Bothrockptarmiganandblackgrousefeedpredominantly onplants,especiallyonleafsandbudsofheather(Ericacea), includingbilberry(Vacciniummyrtillus),mountaincranberry (Vaccinium vitis-idaea) and black crowberry (Empetrum nigrum) as well as dwarf willows (Salix herbacea, Salix retusa)and–especiallyyoungchicks–alsooninsects(Glutz von Blotzheim et al. 1973; Lieser, Zakrzewski, & Sittler, 1997; Bertermann, Weber-Sparenberg, Pechura, Renard,

& Bergmann, 1998; Starling-Westerberg 2001; Beeston, Baines,&Richardson,2005).Habitatsuitabilitymodelsfor thepresenceofbothspeciesintheEuropeanAlpsgenerally reflectthe importanceofpatchyandheterogeneoushabitat structuresforfoodandshelter(Favaron,Scherini,Preatoni, Tosi,&Wauters,2006;Zohmann&Wöss2008;Pattheyetal.

2012).Schweiger,Nopp-Mayr,&Zohmann(2012)further- morehighlighted the importanceof dwarfshrubs for both species,andanthills(reflecting aninsectfood source)for blackgrouse.Whilecurrentdietandhabitatcharacteristics appear to be well known, it remains open how the pre- dictedchanges intemperature, precipitation, reduced (and higher elevated) suitable habitat and changed plant com- position will affect diet and in the long term population trajectories.

Asafirststepwehereaimtoinferhowprecipitationpat- ternsmayaffectsummerdiet,bycomparingdietarychanges along a distinctgradient in precipitationwithin the Swiss canton of Grisons (Frei & Schär 1998; see Fig. 1). Sta- bleisotopes,particularlythecombinationof␦¹⁵Nand␦¹³C isotoperatiosprovideacomprehensivepictureofdietaryrela- tionships: ␦¹⁵Nincreases with each trophic level and can thereforebeusedtoassessthetrophicpositioninthefoodweb (reviewedinCaut,Angulo,&Courchamp,2009).Incontrast,

␦¹³Cvarieswithbed-rockandbetweenC3andC4-plants(Fry 2006).Furthermore,␦¹³Cratiosinplantsdecreasewithrain- fall(Stewart,Turnbull,Schmidt,&Erskine,1995;Ferrio&

Voltas2005)andincreasewithelevation(Körner,Farquhar,

&Roksandic,1988; Vande Water, Leavitt,&Betancourt, 2002).Feathersareafrequentlyanalysedtissueandreflectthe dietduring,orshortlypriortomoult,astheyremainmetaboli- callyinertaftertheirformationandevenafterdeath(Bearhop, Waldron,Votier,&Furness,2002).Blackgrousemoulttheir entireplumage,androckptarmigantheirprimary andsec- ondarywingfeathersduringthesummermonths,towardsthe endofthechickrearingperiod(GlutzvonBlotzheimetal.

1973).Thefeathersamplesanalysedinthisstudytherefore reflectthedietduringsummer.

By analysing precipitation patterns, plant and feather isotopes,we thus aimedto(1) investigatepotential differ- encesinisotopiccompositionandconsequentlydietrelated to regional precipitation patterns. Based on the literature, we expected plant␦¹³C andconsequentlyfeather ␦¹³C to increasealongtheprecipitationgradientwithlongitude,but expectednochangesinplantandfeather␦¹³Cwithlatitude.

We furthermore expected generally higher ␦¹³C valuesin plantsamplesathigheraltitudesandconsequentlyinfeathers ofrockptarmigancomparedtoblackgrouse.

Plant␦¹⁵Nvaluesshouldnotbeaffectedbyprecipitation, and we thereforeexpected nogradient inplant ␦¹⁵Nwith longitudeoraltitude.Wehadnospecificexpectationsasto howprecipitationwouldaffectdietarycompositionof rock ptarmiganandblackgrouse.However,ifprecipitationwould affectthefoodchoiceofeitherofthespecies,weexpectedto seeachangein␦¹⁵Nwithlongitude.

We further investigated (2) intra-specific dietary differ- encesbetweenadultandimmaturebirdsandbetweenadult malesandfemalesinrockptarmigan.Asjuvenileshavebeen described to feedon a moreinsect-rich diet, we expected tofindhigher␦¹⁵Nvaluesinfeathersofimmatures(i.e.the firstsetofprimariesandsecondariesthatisbuiltwhenstill guardedbythehens)comparedtoadults(moultedinsum- meratthesametimeaschickrearing).Finally(3),wetested whetherrockptarmiganandblackgrousedifferintheirdiet.

Duetothedifferencesinaltitudinaldistributionduringsum- mer,weexpectedtofindhigher␦¹³Cvaluesinrockptarmigan thanblackgrouse.Assumingasimilardietinbothspecies, wehoweverexpectedsimilar␦¹⁵Nvaluesinbothspecies.

Materials and methods

Feathersofblackgrouseandrockptarmiganwereobtained fromseveralhuntingdistrictswithinGrisons(Fig.1),during thehuntingseasonbetweenmid-OctobertoendofNovember.

Hunters wereobligedtodeliverfeather samplesfromshot black grouse(secondarywing feathersor bodycoverts;in 2005–2007),androckptarmigan(secondarywingfeathers;

in 2008–2012) tothe Department of Wildlife andFishery ServiceGrison. Featherswerestoredinplasticbags along withinformationaboutageandsex(identifiedfromplumage characteristics). Forblack grouse,the detailed coordinates oftheshotlocationswerealsoregistered,whereasforrock ptarmiganonlythemunicipalitywasnoted.Forsubsequent analysesregardinglocations,wethereforeusedtheprinciple town/villagewithinthemunicipalityforrockptarmigan,but thedetailedlocationforblackgrouse.

Feathersfromblackgrouseweresolelyfrommalebirds, eitheradultorimmature.Feathersfromrockptarmiganwere from both sexes andincluded bothadults andimmatures.

In few cases(N=11 out of 190 feather samples in total), sexor agewas notnoted, andsample sizes thereforevary slightly among analyses. In order to understand potential intra-specificvariationinstableisotoperatiosacrossyears, betweensexes,andage(adultsandimmatures),wechosethe municipalitywiththehighestnumberofshotanimals(Pon- tresina; see location in Fig. 1) andanalysed atotal of 78 samples fromrockptarmigan,equallycoveringbothsexes and age groups from the years 2008 to 2012. To analyse

Fig.1. LocationofSwitzerland(blackframe)andGrisons(blue-greencoloured)withintheEuropeanAlps(insertedplotintop-leftcorner).

Themainfigureshowsthesumofprecipitation(inmm;seelegendonthelefthandside)intheyear2013inGrisonsandsamplelocationsof plants(green),rockptarmigan(red)andblackgrouse(black)feathers.Forthetwogrousespeciesthesizeofthedotsreflectsthenumberof sampledindividualsintheyear2005(blackgrouse)and2009(rockptarmigan,respectively).LukmanierpassandOfenpass(markedwithlarge greendots)arethelocationswhereplantsweresampledmoreintensivelytocompareinterspecificisotopicvariation.Pontresina,thelocation wheremostrockptarmiganwereshot,ishighlightedassamplesfromthislocationwereusedforinter-annualandintra-specificcomparisons ofisotoperatios.AtotalofN=137feathersamplesofrockptarmigan,N=53feathersamplesofblackgrouseandN=197plantsampleswere analysed.Sumofprecipitationasshownhereisbasedonspatialinterpolationofweatherstationdata(accordingtoRhiresYv.1.0.;detailsin Freietal.1998).ThebackgroundmapwasmodifiedbasedonafigureprovidedbyMeteoSwiss.(Forinterpretationofthereferencestocolor inthisfigurelegend,thereaderisreferredtothewebversionofthisarticle.)

thegeographiceffectsandspeciesdifferences,blackgrouse feathers from 2005 (N=53 samples) and rock ptarmigan feathers from 2009 (N=59 samples) from across Grisons (N=19 and 21 municipalities for black grouse and rock ptarmigan,respectively)wereanalysed(Fig.1).

Collectionofplantsamples

Plantswere sampled between10th of July and 23rd of August 2013. Sampling locations were distributed across Grisonsmatchingtheoverallhuntinglocationsofthebirds (Fig.1).Perlocation(e.g.Vilan),wecollectedplantsamples atonetotwodifferentplots, ifpossibleatdifferent eleva- tions(e.g.oneat1900m,andoneat2300m;seeTableA1 fordetailsaboutsampledplantspeciesperlocation).Ateach plot,we collected3–5 samples perplant species,andide- allyfromatleasttwospecies(dependingonavailabilityat the plot), generally onefrom the family Ericacea (mostly bilberry, Vaccinium myrtillus) and the second either from Salicacea (Salix reticulata) orRoseacea (Geummontanum orDryasoctopetala).Eachsampleconsistedofonebranch withseveralleaves,andsampleswerecollectedfromseparate specimensthatgrewatleast3mapartfromeachother.

In orderto estimate the isotopic variation among plant species also within the plant family Ericacea, we covered twolocations(OfenpassandLukmanierpass;seeFig.1)more closelyandanalysedsamplesfrom6and7species,respec- tively.

Stableisotopeanalyses

Plant sampleswere dried inadrying ovenat 50^◦Cfor at least 48h. We ground two leaves per individual plant andmixedthemthoroughly.Sub-samples(ca.0.5mg)were weighed into 0.3mm×0.5mm tin capsulesto the nearest 0.001mg,usingamicro-analyticalbalance.

Forfeather samples, weused the distal endof feathers.

Only feathersfree of visiblecontamination(dirtor blood) wereused.Featherswererinsedwith75%ethanolandsubse- quentlywithdistilledwater,andthendriedinadryingoven at50^◦Cforatleast 24h.Sub-samples of0.8–0.9mgwere weighedintotincapsules.

Sampleswerecombusted inaPyrocube elementalanal- yser. The resulting CO2 and N2 were separated by gas chromatographyandadmittedintotheinletofaMicromass

(Manchester,UK) Isoprime isotoperatio massspectrome- ter(IRMS)fordeterminationof¹³C/¹²Cand¹⁵N/¹⁴Nratios.

Measurements are reportedin ␦-notation (␦¹³C and␦¹⁵N, respectively)relative tothe PeeDee Belemnite (PDB)for carbonandatmosphericN2fornitrogeninpartsperthousand deviations(‰)usingtheformula

δ(‰)=1000×

Rsample

Rstandard−1

Twosulfanilamides(iso-primeinternalstandards)andtwo Casein standards were used for every seven unknowns in sequence.Internallaboratory standards indicatedmeasure- menterrors(SD)of±0.05‰for␦¹³C,0.15‰for␦¹⁵N.

Weatherdata

WeobtainedprecipitationdatafromGrisons(108weather stations;fromtheSwissFederalOfficeofMeteorologyand Climatology,MeteoSwiss)as wellas from66weathersta- tions in adjacent areas within Switzerland, Austria (from Zentralanstaltfür MeteorologieundGeodynamik, ZAMG) andItaly (from AgenziaRegionale perla Protezionedell’

Ambientedella Lombardia,ARPA Lombardia). Wecalcu- latedthesumof precipitationof themonthsAprilthrough toAugust2013,i.e.thegrowthperiodoftheyearinwhich wecollectedplantsforisotopeanalyses.Weusedthesedata toanalyse geographicaldifferences inprecipitationwithin Grisons(seeStatistics,firststep).

Statisticalanalyses

All statistics were performed in R (version 3.1.1; R Core Team, 2014). We conducted linear models (LM) and linear mixed effect models (LMM) using the pack- ageslme4(Bates,Maechler,&Bolker,2011)andlmerTest (Kuznetsova, Brockhoff, & Christensen, 2014). We per- formed backwards-stepwise model selection, subsequently removing non-significant variables from the models. P- values were obtained from likelihood-ratio tests between modelswithandwithoutthefocalvariable.

Inthefirststep,weanalysedpotentialdifferencesiniso- topiccompositionandconsequentlydietarychangesrelated tothe regionalprecipitation pattern.We therefore(I) ana- lysedtheprecipitationpatternfortheyear2013inGrisons, runningaLMwiththesumofprecipitationduringthegrowth period (April–August) as dependent variable. Asexplana- tory variables, we included latitude and longitude of the weatherstationaswellasthetwo-wayinteractionterm(lat- itude*longitude).

Wethen (II) tookplant samples from alllocations into account, andstudied the effects of latitude, longitude and elevation on plant isotopes. We ran LMMsseparately for

␦¹⁵Nand␦¹³Casdependentvariables.Aselevationwassig- nificantlycorrelatedwithlatitudeandlongitude(Pearson’s R=−0.16and0.43,P=0.026and<0.001,respectively),we

conductedmodelsseparatelyforgeographiclocationandele- vationtoavoidcollinearity.Thefirstsetofmodelstherefore contained latitude,longitude andthe interactionterm(lati- tude*longitude)asexplanatorycovariatesandplantspecies asrandomeffect.Thesecondsetofmodelscontainedonly elevationasexplanatoryvariableandplantspeciesasrandom effect.

Forthe twomoreintensivelysampledlocationsof Luk- manierpass andOfenpass, we also tested whether isotope valuesdifferedamongplantspecies.Wethereforeconducted LMMswithplantspeciesasfixedeffectandthestudysiteas randomeffect.

Finally(III),weinvestigatedvariationofrockptarmigan (alldatafrom2009)andblackgrouse(alldatafrom2005)iso- topedatawithlatitudeandlongitude.Again,weranLMMs separatelyfor␦¹⁵Nand␦¹³C.Thestartingglobalmodelcon- tainedspecies(asfixedfactor)andbothlatitudeandlongitude (eachascovariates)andallpossibleinteractiontermsupto thethree-wayinteractionbetweenspecies,latitudeandlon- gitude(asexplanatoryvariables),aswellassexandage(as independentrandomvariables).

In addition to these regional effects, we analysed in a secondsteppotentialintra-specificdifferencesinbothrock ptarmiganandblackgrouse.Forrockptarmigan,weuseda separatedataset whichcontaineddatafromthe years2008 to 2012shot withinthe range of the municipalityof Pon- tresina.Weusedthisdatasettoinvestigatesex,ageandyear differences.LMsthereforecontainedsex,ageandyear(each asfixedfactor)andallpossibletwo-andthree-wayinterac- tions.Forblackgrouse,weexclusivelyused thedatafrom 2005fromacrossGrisons.

Finally, in the third and last step, we analysed poten- tial species differences betweenrockptarmiganand black grouse,usingaLMwithspeciesastheonlyexplanatoryfac- tor, applied tothe dataset of feather isotope datasampled across Grisons inthe years2005 (adultblack grouse)and 2009(adultrockptarmigan).

Results

Geographicaleffectsalongaprecipitation gradient

Within Grisons, precipitation during the growth sea- son 2013 (April–August) showed a significant interac- tion between latitude and longitude (LMM: F1=12.12, P<0.001). Tested separately, precipitationdecreased with latitude(LMM:F1=9.90,P=0.002)andlongitude(LMM:

F1=90.04, P<0.001), thusthesouthern andwestern parts of the canton received more precipitation than the north- ernandeasternparts,coincidingwiththeannualpatternof precipitation(Fig.1).

Withinthesamegeographicalrange,plant␦¹³Cincreased significantly with elevation (LMM: F1=28.65, P<0.001) (Fig. 2)and withlongitude,i.e. from westto east(LMM:

Fig.2. Effectsofelevationon␦¹³Cand␦¹⁵Nofplants.Regression linesareshownforsignificanteffectsonly.

F1=23.98,P<0.001),whiletherewasnosignificanteffect oflatitude(LMM:F1=3.19,P=0.090)(Fig.3).Plant␦¹⁵N valueswerenot significantlyaffectedbyelevation (LMM:

F1=0.07, P=0.800) (Fig. 2), latitude (LMM: F1=2.09, P=0.090)orlongitude(LMM:F1=0.38,P=0.536)(Fig.4).

Focussingonthevariationamongplantspecies,wefound asignificant specieseffectonboth␦¹³Cand␦¹⁵N(LMM:

F10=11.76,P<0.001andF10=2.36,P=0.006for␦¹³Cand

␦¹⁵N,respectively)atthetwointensivelysampledlocations ofLukmanierpassandOfenpass(TableA1).Speciesdiffer- encesin␦¹³Cand␦¹⁵Nwerealsopresentwithinthefamily Ericacea(LMM:F7=13.04and2.07,P<0.001and0.028, respectively),anddifferencesfor␦¹³Cremainedsignificant evenwithin the samegenus: Mountaincranberry, V.vitis- idaea,andbilberry,V.myrtillus,sampledatthesamestudy plot(i.e.samegeographiclocationandelevation)differedsig- nificantlyintheir␦¹³Cvalues(LMM:F1=20.80,P=0.002), butnotintheir␦¹⁵Nvalues(LMM:F1=0.99,P=0.348).

Analysing rock ptarmigan and black grouse data from across Grisons, we obtained a significant three-wayinter- actiontermbetweenspecies,latitudeandlongitudeforboth

␦¹³C(LMM:F1=3.77,P=0.024)and␦¹⁵Nvalues(LMM:

F1=4.35,P=0.018).Wethereforecontinuedwithseparate analysesforbothspecies.

In rockptarmigan, feather␦¹³Cwasindependentof lat- itude (LMM: F1=0.52, P=0.444) and longitude (LMM:

F1=0.122,P=0.717;Fig.3).Feather␦¹⁵Nwasindependent of latitude(LMM:F1=0.08,P=0.906)butincreasedwith longitude(LMM:F1=6.11,P=0.013;Fig.4).

Inblackgrouse,theinteractiontermoflatitudeandlongi- tudehadasignificanteffectonfeather␦¹³C(LMM:F1=7.69, P=0.005).Analysedinseparatemodels,␦¹³Cincreasedwith longitude(LMM:F1=6.99,P=0.009)butwasnotaffected bylatitude(LMM:F1=0.65,P=0.412;Fig.3).Feather␦¹⁵N wasindependentoflatitude(LMM:F1=1.33,P=0.243)and longitude(LMM:F1=0.12,P=0.729;Fig.4).

Intra-specificdifferencesinrockptarmiganand blackgrouse

Wetestedintra-specificdifferencesinrockptarmiganwith a 4-year dataset from the municipality of Pontresina and foundthatfeather␦¹³Cvaluesweremarginallylowerinmales thanfemales (LM:F1=4.44,P=0.039;Fig.A1).Further- more,theinteractionbetweenyearandage(LM:F1=2.59, P=0.045;Fig. A2) was significant. Albeit significant, the overalldifferenceswereratherweak(Figs.A1andA2).Rock ptarmiganfeather ␦¹⁵Nvalueswere notaffectedby either year,sexorageoranyinteractionterm(LM:allF1≤1.69, allP≥0.164).

InblackgrousesampledacrossGrisons,feather␦¹³Cand

␦¹⁵Nvaluesdidnotdifferbetweenadultandimmaturemales (LM:F1=0.07and0.01,P=0.798and0.986for␦¹³Cand

␦¹⁵N,respectively).

Speciesdifferencesbetweenrockptarmiganand blackgrouse

Overall,adultrockptarmiganhadsignificantlyhigher␦¹³C values(LM:F1=77.36, P<0.001)andsignificantlylower

␦¹⁵Nvalues(LM:F1=118.62,P<0.001)thanadult black grouse,withisotopicvaluesofbothspeciesshowingnoover- lap(Fig.5).

Discussion

Effectoflatitudeandlongitudealongthe precipitationgradient

Grisons shows a distinct precipitation gradient, with decreasingspringandsummerrainfallsfromwesttoeast.In agreementwithourexpectation,plant␦¹³Cincreasedwith longitude,butnotlatitude,andnoeffectofeitherlatitudeor longitude wasfoundfor plant␦¹⁵N.Thesamepattern was foundforblackgrousefeathers,suggestingthatthedietary compositionofblack grousedidnotchange alongthepre- cipitationgradientwithlongitudewithinthestudyarea.

Fig.3. Effectsoflatitudeandlongitudeon␦¹³Cofplants,rockptarmiganandblackgrousefeathers.Notethatthescalingfor␦¹³Cdiffers betweentheplantsandthetwogrousespecies.Regressionlinesareshownforsignificanteffectsonly.

Incontrast,inrockptarmigan,wefoundadifferenteffect:

While␦¹³Cinfeathersdidnotdifferwitheitherlatitudeor longitude,␦¹⁵Nincreasedwithlongitude.The lattermight suggest that the proportion of insects in the rock ptarmi- gandiet increased from west to east, andtherefore along theprecipitationgradient.Albeitsignificant,theeffectitself wasrathersmallandmightonitsownbebiologicallyhardly meaningful.Inaddition,however,thelongitudinaleffectof plant␦¹³Cwasnotreflectedinrockptarmiganfeatheriso- topes. Considering that rock ptarmigandiet appears tobe based even moreon plants than that of black grouse (for whichtheeffectwasvisible),thisissurprising.Potentially, thesecombinedeffectsin␦¹³Cand␦¹⁵Nthereforedosuggest achangeindietarycompositionand/orfoodsourcesofrock ptarmiganoverthelongitudinalprecipitationgradient.

Intra-specificvariationinisotopes

Againstourexpectations,wefoundnoage-dependentdif- ferencesindietary compositionineitherrockptarmiganor black grouse.Although invertebratediet is expectedtobe commoninimmatureindividuals,wefoundnodifferencesin

␦¹⁵N(whichwouldhaveindicatedamoreinvertebrate-rich diet in immatures).While young black grouse in Norway and northernEngland took substantiallymore insect prey

compared to adults (Starling-Westerberg 2001; Wegge &

Kastdalen2008),wearenotawareof anystudiesfromthe European Alps that comparedthe diet betweenadultsand juveniles.Inrockptarmigan,earlierstudiesfromGreenland and the Alps suggested that dietary segregation with age mightbelessstrongcomparedtoblackgrouse(Lieseretal.

1997 andliterature therein). Furthermore, potential differ- ences inthe dietmightdecrease withageofthe juveniles, andmaynotbepresentany moreduringformationofsec- ondarywingfeathers(whichourisotopeanalyseswerebased upon).

Inter-specificdifferencesintheisotopicvalues anddiet

Blackgrousehadsignificantlylower␦¹³Candhigher␦¹⁵N levelsthanrockptarmigan,withnooverlapofisotopicval- ues.Asrockptarmiganaredistributedathigheraltitudesthan black grouse,andbasedonourexpectations (andfindings) thatplant␦¹³Cincreaseswithelevation,weanticipatedtofind thehere-observedspecies-segregationin␦¹³Cindependentof dietarypreferencesofbothspecies.Assumingasimilardiet inbothspecies,weexpectedtofindsimilar␦¹⁵Nvaluesin bothspecies.Instead,blackgrousefeathershadonaverage 2.5‰higher␦¹⁵Nvaluesthanrockptarmiganfeathers.This

Fig.4. Effectsoflatitudeandlongitudeon␦¹⁵Nofplants,rockptarmiganandblackgrousefeathers.Notethatthescalingfor␦¹⁵Ndiffers betweentheplantsandthetwogrousespecies.Regressionlinesareshownforsignificanteffectsonly.

Fig.5. Stablenitrogenandcarbonisotoperatios(‰)ofadultrock ptarmiganandblackgrouse.Eachpointrepresentsoneindividual adultbirdfromGrisons.N=38rockptarmiganand33blackgrouse, respectively.

differencecannotbeascribedtoaneffectofaltitude,asplant isotopesdidnotdifferin␦¹⁵Nwithelevation.Theoretically, thespeciesdifferencesin␦¹⁵Ncouldbeexplainedbyblack grousefeedingconsistentlyonplantspecieswithhigher␦¹⁵N

valuescomparedtorockptarmigan.However,variabilityin

␦¹⁵Nwasalsolargewithinplantspecies,evenwithinthesame studyplots,i.e.withinarangeofafewmetres(seestandard deviationsshowninTableA1).Itthereforeappearsunlikely that black grouseconsistently selectedfor plantspecimen withhigh␦¹⁵N,whereasrockptarmigandidtheopposite.A morelikelyexplanationforboththehigher␦¹⁵Nvaluesin blackgrouseandthelargerintra-specificvariationin␦¹⁵Nin thisspecieswouldbethatblackgrousefeedonahigherpro- portionofinvertebratescomparedtorockptarmigan.Along thefoodchain,␦¹⁵Nincreaseswitheachtrophicstep(DeNiro

&Epstein1981;Minagawa&Wada1984).Thistrophicfrac- tionationrangesbetweenapproximately2‰ and5‰(Post 2002).Thedifferencein␦¹⁵Nbetweenblackgrouseandrock ptarmiganthereforerepresentedadifferencebyabouthalfto one trophic level, suggestingthat invertebrates make upa considerableamountofdietinblackgrouse.Incontrast,diet inrockptarmigancanbeexpectedtobebasedprimarilyon plantsduetotherathersmalldifference(onaverage2.22‰) in␦¹⁵Nbetweenanalysedplantmaterialandrockptarmigan feathers.

The literature so far ascribed a similar, mainly plant- baseddiettoadultsofbothofourstudyspecies(Glutzvon Blotzheimetal.1973;Lieseretal.1997;Bertermannetal.

1998;Starling-Westerberg2001;Beestonetal.2005).While

weareunabletoidentifywithcertaintywhetheradifferential plantdietortheproportionofinvertebratescausethediffer- encesin␦¹⁵N,ourdataclearlysuggestadietarysegregation betweenblackgrouseandrockptarmigan,whichhasnotbeen describedpreviously.

Potentialcaveatsofthisstudy

Weconductedstableisotopeanalysesonlyforalimited numberof plant specimen andplantspecies, not covering theentirefoodwebofrockptarmiganandblackgrouse.In particular,wedidnotsampleanyinvertebrates,which–with hindsight–couldhavehelpedwiththeinterpretationofour results.Variationinboth␦¹³Cand␦¹⁵Nwithinandbetween plantspecieswaslarge,alsowithinspeciesandwithinstudy plots(seeTableA1),andvariationwouldlikelybeevenlarger underinclusionofmoreplantspecimen.Duetothisstrong variationandthehighoverlapofisotopevaluesamongplant species,andfurtherlackofknowledgeaboutthefractionation factorsbetweenisotopicratiosinthe birds’foodandtheir feathers,wedecided againstrunningstableisotopemixing modelsas resultswould come withalargelevel of uncer- tainty.Consequently,wewere,however,notabletoestimate specificdietarycomponentsinthedietofrockptarmiganand blackgrouse.

Oursamplingdesignwasfurthermoresuboptimalinthat plants,rockptarmiganandblack grousefeathers hadtobe sampledinthree differentyears. Wetherefore cannotrule out entirely that long-term year-effects may have biased ourresults.However, wewould like toemphasisethat (1) therewerenosubstantialandbiologicallymeaningfulyear- differences in either ␦¹³C or ␦¹⁵N in feathers from rock ptarmigan within the municipality of Pontresina; and (2) accordingtoMeteoSwisstheprecipitationgradientwithlon- gitude inGrisons waspresent across the entire period for whichsamples from either birds or plants were obtained.

Wethereforeassumethat despite thesuboptimal sampling design, our finding of dietary segregation between rock ptarmiganandblackgrouseisrobust.

Conclusions/implicationsofthisstudy

Alpinewildlifeisseverelyaffectedbyanthropogenicinflu- ences,fromlandusepatternstoglobalclimatechangethat willaffecttemperatureandprecipitationpatternsintheAlps.

Oneaimofthisstudywasthereforetoinvestigatethedietary changes along a precipitation gradient within the central European Alps in both rock ptarmiganand black grouse.

Overall, ourdata suggestedapotential effectof precipita- tion onthe diet of rockptarmiganand noeffect onblack grouse.Themoresignificantandslightlyunexpectedresults ofthisstudywere,however,thedietarysegregationofrock ptarmiganandblackgrouse.

Acknowledgements

SaskiaRehse, CorinnaWaider,Claudia GreisandWolf- gang Kornberger helped with stable isotope analyses and Marc Mischke with generating the GIS plots. Thanks to DanSuriforhelpfuldiscussionsaboutprecipitationdataand Englishproofreading.WethankProf.K.O.Rothhauptandthe staffattheLimnologicalInstituteattheUniversityofKon- stanzforlogisticalsupport.ThisstudywasfundedbytheOtto WolffStiftung.NDwassupportedbytheFWO-Flandersdur- ingwritingofthismanuscript(grantnumbers1265414Nand 12Q6915N).

Appendix A. Supplementary data

Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/

j.baae.2016.04.007.

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