J Anim Ecol. 2018;87:87–100. wileyonlinelibrary.com/journal/jane  | 87© 2017 The Authors. Journal of Animal Ecology © 2017 British Ecological Society

Received:18December2016  |  Accepted:1June2017DOI: 10.1111/1365-2656.12720

S Y N T H E S I S

Using experimentation to understand the 10- year snowshoe hare cycle in the boreal forest of North America

Charles J. Krebs1  | Rudy Boonstra2 | Stan Boutin3

1DepartmentofZoology,UniversityofBritishColumbia,Vancouver,BC,Canada2DepartmentofBiologicalSciences,UniversityofTorontoScarborough,Toronto,ON,Canada3DepartmentofBiologicalSciences,UniversityofAlberta,Edmonton,AB,Canada

CorrespondenceCharlesJ.KrebsEmail:krebs@zoology.ubc.ca

Funding informationNaturalSciencesandEngineeringResearchCouncilofCanada

HandlingEditor:KenWilson

Abstract1. PopulationcycleshavelongfascinatedecologistsfromthetimeofCharlesEltoninthe1920s.Thediscoveryoflargepopulationfluctuationsinundisturbedecosys-temschallengedtheideathatpristinenaturewasinastateofbalance.The10-yearcycleofsnowshoehares(Lepus americanusErxleben)acrosstheborealforestsofCanada and Alaska is a classic cycle, recognized by fur traders for more than300years.

2. Since the1930s, ecologists have investigated themechanisms thatmight causethesecycles.Proposedcausalmechanismshavevariedfromsunspotstofoodsup-plies,parasites,diseases,predationandsocialbehaviour.Boththebirthrateandthedeathratechangedramaticallyoverthecycle.Socialbehaviourwaseliminatedasapossiblecausebecausesnowshoeharesarenotterritorialanddonotcommitinfanticide.

3. Sincethe1960s,large-scalemanipulativeexperimentshavebeenusedtodiscoverthemajorlimitingfactors.Foodsupplyandpredationquicklybecamerecognizedaspotential key factors causing thecycle.Experiments adding foodand restrictingpredatoraccesstofieldpopulationshavebeendecisiveinpinpointingpredationasthekeymechanismcausingthesefluctuations.

4. Theimmediatecauseofdeathofmostsnowshoeharesispredationbyavarietyofpredators,includingtheCanadalynx(Lynx canadensisKerr).Thecollapseinthere-productiverateisnotduetofoodshortageaswasoriginallythought,butisaresultofchronicstressfrompredatorchases.

5. Fivemajorissuesremainunresolved.First,whatisthenatureofthepredator-in-ducedmemorythatresultsintheprolongedlowphaseofthecycle?Second,whydoharecyclesformatravellingwave,startinginthecentreoftheborealforestinSaskatchewanandtravellingacrosswesternCanadaandAlaska?Third,whydoestheamplitudeofthecyclevarygreatlyfromonecycletothenextinthesamearea?Fourth,dothesamemechanismsofpopulationlimitationapplytosnowshoeharesineasternNorthAmericanor insimilarecosystemsacrossSiberia?Finally,whateffectwill climaticwarminghaveonall theabove issues?Theanswers to thesequestionsremainforfuturegenerationsofbiologiststodetermine.

K E Y W O R D S

borealforest,foodshortage,Kluaneecosystem,Lepus americanus,predation,sublethalstress,synchrony,travellingwaves,Yukon

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1  | INTRODUCTION

Populationfluctuationshavealwayscaptivatedpeoplepartlybecausetheycanaffectlivelihoodsaspestspeciesthatattackcropsorasgameanimalsthatprovidemeatorfurs.WhenCharlesEltondiscoveredthedetaileddatacompiledbytheHudsonBayCompanyonfurs tradedfromdifferent parts ofCanada since 1673, he quickly realized thatthesedatawereatvariancewiththecommonbeliefinthestabilityofnaturalsystemsnotsubjecttohumandisturbance.Eltonbeganwhathasbecomeatidalwaveofliteratureonpopulationcyclesandtheircausesandconsequencesforecosystems.Thenaturalvariationinde-mographyexhibitedbycyclicpopulationshasprovenextremelyusefulforunderstanding thecomplex interplaybetweenplants,herbivoresandpredators.

The10-yearcycleofsnowshoeharesandtheirpredatorsshowedupclearlyinfurreturnsfromacrossCanadaandAlaska,andpresenteditselfasatestcaseforunderstandingoneparticularpopulationcyclewhich had a 300-year historywritten in fur returns on a continen-talscale.Thelistofecologicalfactorsthatcouldproduceacyclewasquicklyidentifiedsincethemechanismshadtoshowatime-lagintheireffects.Overgrazingandfoodshortagefitsthisprofile,asdoespreda-tionmortality,parasitesanddiseases.Otherfactorslikesunspotswerebroughtintothepicturebutquicklydismissedaspotentialagentsbe-cause their temporal fluctuationsdidnotmatch the snowshoeharecyclictime-scale.

Earlywork byGreen and Larson (1938) andGreen, Larson, andBell(1939)postulatedthatastressdiseasetheycalled“shockdisease”wasthecauseofcyclicdeclines.Thisearlyworkwasdismissedasanartefactofstudiesdoneonhares incrowded laboratoryrooms.Butthegeneral ideaofGreenandLarson(1938)thatharesmightsufferfromsomeintrinsicailmentwasdormantuntil60yearslaterwhenitwasbroughtbackinstudiesofchronicstress(Boonstra,2013)asde-scribedbelow.

In1948,WilliamRowan,theHeadofZoologyattheUniversityofAlberta,declaredthat the10-yearcyclewasthe“outstandingprob-lemofCanadianconservation.”HestimulatedLloydKeithtocarryoutaseriesofstudiesonthesnowshoeharecycleinAlberta,beginninghiscareerwithanearlybookoncycles(Keith,1963).LloydKeithwasconvincedthattheharecyclewasdrivenbytwofactors,foodshortageinwinter,whichdepressedreproduction,andpredationinthedeclinephase.Heandhisstudents’researchincentralAlbertawasthefirsttolayafirmquantitativefoundationtothedemographyoftheharecycle(Keith,1983;Keith&Windberg,1978).

Fromthisearlierresearch,welaunchedourresearchprogrammein1976intheKluaneRegionoftheYukon.Previousresearchhadlaidoutfourclearhypothesestotestexperimentally:

1. The hare cycle was caused by winter food shortage and thedelayedrecoveryofwinterbrowsedamagedbyexcessivebrows-ing by hares.

2. Theharecyclewascausedbychangesinfoodqualityasaresultofheavybrowsingbypeakharedensitieswhichtriggeredanincreaseinsecondarycompoundproductionbytheplants.

3. Theharecyclewascausedbyheavypredationandthetime-lagin-herentinpredatorratesofpopulationgrowthrelativetothatofthehares.

4. Theharecyclewascausedbybothfoodandpredators,withfoodshortageatthepeakfollowedbyheavypredationinthedecline.

Our approach consisted of obtaining detailed information on de-mographicparameterscombinedwithmeasuresofquantityandqualityofharefoodinthewinterandestimatesofkillratesofharepredatorstotestpredictionsfollowingfromeachhypothesis.Wewentonestepfurther, however, byexperimentallymanipulating foodavailability andpredationrates.Ourapproachwasnotguidedbyapriorimathematicalmodelsbecausetherewasonlylimitedempiricalinformationtoparame-terizesuchmodelsandthemanipulationsweretheobviousonesbasedontheLloydKeithwork.

2  | MATERIALS AND METHODS

Allourstudiesonsnowshoehareswereconductedby livetrappingand radiocollaring of individuals. The details of thesemethods andthoseforradiotelemetryhavebeendescribedindetailinHodgesetal.(2001).PopulationestimatesofalltheharedatapresentedherewerecalculatedinDENSITY4and5(Efford,2009).Themajorexperimentsaredescribed indetail inBoutinetal. (2001),andmuchmoredetailaboutour generalmethods is given inKrebs,Boutin, andBoonstra(2001).

2.1 | Natural history of the snowshoe hare

Criticaltounderstandingthepopulationdynamicsofsnowshoeharesisknowledgeoftheirlifehistoryandtheconstraintsoftheirdietandhabitat. These hares are the major herbivores in the boreal forestecosystem,both intermsofbiomassandof impact (Boonstraetal.,2016).Wesummarizethekeyfeaturesof theirnaturalhistoryhere(seeHodges,2000forreferences).Theyarepurewhiteinwinterandbrown insummer.Allbreedingtakesplace insummer,withamaxi-mum of four litters being produced. Females breed synchronouslyand engage in post-partum insemination. The gestation period is35–37days,withthefirstlitter(borninlateMayintheYukon)aver-agingthreeleverets,thesecondfive,andthethirdandfourth(iftheyhavethem)betweenthreeandfive leverets.Youngdonotbreedintheiryearofbirth.Althoughtherareharecanlive7years,mostliveveryshortlives(theaveragelifespanis1year),withalmostallmor-talitybeingattributedtopredation (Boutin,Krebs,Sinclair,&Smith,1986;Hodgesetal.,2001;Keith&Windberg,1978;Murray,Keith,&Cary,1998),and70%ofbreedingfemalesbeingyearlings.Virtuallyallavianandmammalianpredatorsintheborealforesteathares(seethefoodweb,Figure6),witheventhegranivoreandherbivore(redsquirrelsandArcticgroundsquirrelsrespectively)eatinghareleveretsinsummer.Inwinter,snowshoeharesarebasicallytheonlypreyforpredatorstoeat,sinceredsquirrelsaremuchlessvulnerableduetoreducedactivity,groundsquirrelshibernate,grousearerelativelyrare

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andsmallmammalsliveinthesubniveanspacebelowthesnow.Harediet inwinter is largely restricted to the twigsof tall shrubs (dwarfbirchBetula glandulosa and willow Salix glauca)andtheendsofsprucebranchesavailableabovethesnowpack,butinsummerincludesforbs,grasses,leavesandsomewoodybrowse.Theavailabilityofbrowseinthewinterisnotonlycomplexanddynamicaschangingsnowdepthallowsharestoaccesstwigsatgreaterheightsbutitalsomakestwigsinaccessibleasharesdonotburrowintosnowtoaccesscoveredtwigs(Keith,Cary,Rongstad,&Brittingham,1984).Deathsduringwinter,evenduringthepeakanddecline,arenotdrivenbystarvationcausedbyabsolute foodshortage,but ratherby increasingpredation rates(Keithetal.,1984).

2.2 | Our experimental results

2.2.1 | Food addition experiments

In1976,wedecidedtotestthesimplesthypothesisforharecycles,thatitwasaresultofwinterfoodshortage.Wesetoutthree10by10grids(30-mspacingoflivetrapstations,7.3ha)forwinterfeedingofcommercialrabbitchow(Krebs,Gilbert,Boutin,Sinclair,&Smith,1986) for the period from1977 to1984.Oneof the twogrids onislandswastoodifficulttoprovisioninwinterandwehadtodiscardit.Wehadmanyproblemswithdisturbances to feedingstationsbybearsandmoosesotheseexperimentswerenotperfect.Theywere,however,mostconsistentwiththehypothesisthatwinterfoodshort-agewasnotnecessaryforsnowshoeharedeclinesbecausealthoughthefoodadditionservedtoincreasedensityduringtheincreaseandpeakphases,itfailedtostoptheharedecline.Wewerecriticizedforthesefeedingexperimentsbecauseweusedartificialhigh-qualityrab-bitchowasfoodandwepusheddensitiestoabovenormal.Toassessthevalidityofthesecriticismswecarriedoutanotherexperimentoffeedingharesinwinteronnaturalfood.Harescompletelydebarkandconsumethetwigsoftreesthatblowdownnaturally.Sowecutdownlargewhite spruce (Picea glauca (Moench)Voss)andaspen (Populus tremuloidesMichx.)treestofeedharesona9-haplotinwinter(Krebs,Boutin,&Gilbert,1986).Control andmanipulatedharepopulationsdeclinedinunisonwithnomeasurableeffectoftheextranaturalfoodprovidedinthedecline(Figure1).Wedecidedthat,whilewinterfoodisveryimportanttohares,itwasnotthelimitingfactorintheKluaneborealforestintheseyears.Wealsofoundthattheproximatecauseof virtually all the mortalities of our sample of radiocollared harescouldbeattributedtopredation(Boutinetal.,1986)whichmatchedthefindingsbyKeithetal.(1984)studyingaharecrashinRochester,Alberta.Thus,wehadtworeplicatesofaharecrashpointingtopreda-tionasthecausalagent.

2.2.2 | Food quality experiments

Thesecondhypothesispostulatingfoodqualityasadriveroftheharecyclehasbeenmorecontroversialanddifficulttotest.Bryant(1981)showed that severebrowsing inwinter increased the level of toxicsecondarycompoundsinfourspeciesofdeciduoustreesinAlaskaand

thatthecarry-overofseverebrowsingcouldinfluencethesnowshoeharecycleviafoodquality.FoxandBryant(1984)postulatedthatin-creasesinsecondaryplantchemicalsafterheavybrowsingresultedinhighlevelsfor2–3yearsafterbrowsingdamage,andthistimedelaycouldbeadelayeddensity-dependent factor ingeneratingharecy-cles via changes in food quality. Sinclair, Krebs, Smith, and Boutin(1988)testedthesecondaryplantchemistryhypothesisbymeasuringphenols and resins inwinter foodplantsoveronehare cycle.Theyfoundthat,contrarytothepredictionsofthishypothesis,secondarycompoundsdecreasedfromtheincreasephasetothepeakphaseandintothedeclineoftheharecycle.Whilesecondarychemicalshadastronginfluenceonfoodchoicebyhares(Rodgers&Sinclair,1997),foodqualitydidnotappeartobealimitingfactorforharepopulationfluctuations.Thecomplexitiesofplantsecondarycompoundeffectsonherbivoresurgescautioninreachingthisconclusion(Torregrossa&Dearing,2009)andmoreresearchisneededinotherpartsoftheborealforest.

2.2.3 | Food addition and predator reduction experiments

It is alwayspossible that a combinationof factorsdeterminespop-ulationgrowth rates,hence,during thenext cycle (1986–1996)wedecidedtomanipulatebothfoodandpredation.Wefedthreelargerlive trappinggrids (20×20trappoints,30-mspacing,32.5ha)con-tinuouslyyear-roundwithcommercialrabbitchowspreadbyaferti-lizerspreader(Boutinetal.,2001).Wesurroundedoneofthesegridswitha2-m-highelectrified fencearound1km2 tokeepmammalianpredatorsout.We couldnot keep avianpredatorsout, so thiswasa predator reduction experiment, not a complete predator removal

F IGURE  1 NaturalfeedingexperimentonsnowshoeharesatKluaneLake,Yukon,duringapopulationdecline,1981–1984.Twocontroltrappingareas(redandbluesymbols)weremonitoreduntilOctober1981whenthefeedingexperimentbeganononearea(symbols)withwinterfeedingoffelledwhitespruceandaspentrees(darkgreensymbols,Krebs,Boutin,etal.,1986).Feedingcontinuedduringthefollowingthreewinterswithnoeffectontherateofpopulationdecline

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symbols, Krebs, Boutin & Gilbert7

winters with no effect on the rate of population decline. 8

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manipulation.Webuiltasecondelectrifiedfencearoundanotherareatotrytomeasuretheimpactofmammalianpredatorremovalalone.Wefertilizedtwootherlargeareas(1km2)withcommercialNPKferti-lizertotestthebottom-upmodelofregulation.AlltheseexperimentsaredescribedindetailinKrebsetal.(2001).

The results surprised us (Krebs etal., 1995) and a synopsis ofthese10-yearexperimentsisillustratedinFigure2.Feedingharesap-proximatelytripledpopulationdensitybutdidnotaffectthedecline(as illustrated earlier in Figure1). Density increase in feeding areaswaslargelybyimmigrationratherthanbyincreasedreproductivesuc-cess.The largest effectoccurredon the combined food+predatorreductionarea,wheredensitiesreachedabout11timesthecontrolvalues at the cyclic peak. Statistically this showsan interactionbe-tweenfoodandpredation.But thiswasapuzzlebecausewecouldnotdetectanyindicationthatwinterfoodsupplieswereinsufficientoncontrolareas(Hodges,Boonstra,&Krebs,2006;Hodges,Stefan,&Gillis,1999).Populationdeclinesinharesaretheresultofseverelydecreasedsurvival ratesduringthecrashandoneofourobjectiveswithourexperimentswastoseeifwecouldmaintainsurvivalratestopreventthedecline.Althoughweimprovedsurvivalonallourtreat-ments,themaximumeffectwasseenonthecombinedfood+pred-atorreductionarea(Figure3)wheresurvivalrateswerehighenoughtomaintaindensitiesatpeakcontrollevelswellaftertheotherareashadcrashed.

Aswithourstudiesofthepreviouscyclewefoundthattheproxi-matecauseofvirtuallyalladultharemortalitywaspredation.Thus,theevidencecontinuedtobuildforpredationratherthanfoodshortageasbeinganecessarydriveroftheharecycle.Ourexperimentsprovedconclusivelythathigh-qualityfoodcouldnotkeepharesfromthejawsandtalonsoftheirpredatorsnordidharesdieofstarvationwhenpro-tectedfrompredators.

Ourexperimentalapproachtotestingtheroleoffoodandpreda-tion in theharecyclehasbeencriticizedon several fronts. Logistics

preventedusfromreplicatingthe importantmammalianpredatorre-movaltreatment.Wewerefacedwithadilemma;replicatethepredatorfenceoraddthe interaction treatmentof foodsupplementationandpredatorexclusion.Wedidhavemultiplecontemporarycontrolpop-ulationsplusthedetaileddemographicinformationcollectedinprevi-ouscyclesascontexttocompareourexperimentalresultsbutapuristwouldarguethatthemajordifferencesweobservedcouldhavebeenduetounknowninherentdifferencesbetweencontrolandexperimen-talsites.Onlyfurtherreplicationwillresolvethisissue.Wealsocouldnotcontrolhareorpredatormovements inandoutofourtreatmentareaswhich affected density and survival estimates (Turchin, 2003).Weallowedharestomovefreelyinandoutofthepredatorfencesandfoodsupplementedareasfromfearofcreatinga“fenceeffect”butwefencedareasthreetimesthesizeofourtrappinggridstotrytopreventdispersaloutofthefence.Manyofourradiocollaredanimalsstillmovedoutsideofthefencewheretheywerekilledbypredators.Itisalsolikelythatpredatorsspatiallyaggregatedwhereourtreatmentscreatedhighharedensities,especiallyasthepopulationdeclinecontinued.

Wehavecontinuedtomonitorthreecontrolgridssincethemajorprojectof1986–1996ended,sothatwenowhavea41-yearrecordofsnowshoeharenumbersinthispartoftheYukon.Figure4illustratesthesequenceofharedensitiesforcontrolareasatKluane.Therehasbeenanirregularbutobservabletrendtolowerandlowerpeakharedensitiesovertheperiodfrom1976to2016.TraditionalknowledgefromKluaneFirstNationspeoplereportedtousthatthe1970–1971peakwasevenhigherthanthe1980–1981peak.Thecontinuedde-clineinharepeaknumbersoverthistimehasbeenaccompaniedbyacontinual increase inbirchandwillowshrubsthatarethebasisofthewinterharediet.Grabowski(2015)showedthatstandingbiomassofdwarfbirchapproximatelydoubledbetweenthe1987–1994sam-pling period and 2014,while greywillow (Salix glauca L.) increasedabout50%inbiomassduringthattime.Thecauseofincreasedshrubgrowthwasprobablyamixtureofreducedoverwinterharebrowsing,increasinglightlevelscausedbywhitesprucetreemortalityfromthe

F IGURE  2 Ratioofpopulationdensitiesforthefourexperimentaltreatmentstoaveragecontrolpopulationdensitiesatthesamephaseoftheharecycle.Ifthereisnotreatmenteffect,weexpectaratioof1.0.Duringthepeakanddeclinephases,themammalianpredatorexclosuredoubleddensity,foodadditiontripleddensity,andthecombinedtreatmentoffoodadditionandpredatorreductionincreaseddensity11-fold

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F IGURE  3 Annualsurvivalrates(95%CL)foradultsnowshoehareswithradiocollarsduringthedeclinephaseofthecyclefromautumn1990toautumn1992.Samplesizesrangedfrom197to278individualsfortheseestimates(AfterKrebsetal.,1995)

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spruce bark beetle (Dendroctonus rufipennis (Kirby)) outbreak (Berg,Henry,Fastie,DeVolder,&Matsuoka,2006)andawarmingclimate.From 1985 to 2016 in the Kluane areaMay average temperatureshavebeen increased1.5°C,andmeanJune toAugust temperatureshave increased 0.3°C (data from Haines Junction MeteorologicalStation,EnvironmentCanada).Earlywintertemperatures(OctobertoDecember) have increased slightly (0.44°C) in these31years,whilelatewinteraveragetemperatures (JanuarytoMarch)have increased2.8°C.Thus,theclimateintheKluaneareaiswarmingbutthewarmingisunevenwithslightsummerwarmingandstrongerwinterwarming,allcompoundedbyhighvariabilityfromyeartoyear.

2.2.4 | Alternative hypotheses for the decline in reproductive rates

CaryandKeith(1979)hadshowninanelegantstudythatharerepro-ductiveoutputcollapsedoverthecyclebutthecollapsebegan2yearspriortoharepeakdensityandcontinuedthroughthedeclinephase.Stefan and Krebs (2001) repeated these observations for Kluanehares.Theproblemthenbecamehowtoexplainacollapseinrepro-ductiveratesintheabsenceofobservablefoodlimitation.Eitherwehadinsufficientinformationonaccesstofoodorfoodquality,orsomeother process reduced reproductive rates. Boonstra and Singleton(1993)andBoonstra,Hik,Singleton,andTinnikov(1998)foundthathareswereseverelystressedduringthepopulationdeclineandpos-tulatedthatstresswasboththeproximatecauseofthereproductivecollapse and the long-term cause of the lowphase (acting throughmaternaleffects),andthatalikelysourceofstresswastheactionofpredatorssearchingforharestoconsume.Thissuggestionarrivedatacriticaltimebecausenewnon-invasivemethodshadbeendevelopedtomeasurestressinwildmammalswithouthavingtoregularlycollectbloodsamples(Sheriff,Dantzer,Delehanty,Palme,&Boonstra,2011).

The hypothesis that predator-induced stress caused the repro-ductive collapse was tested experimentally and observationally bySheriff,Krebs,andBoonstra(2009,2010,2011),whomeasuredstresslevels bymeans of both plasma cortisol levels and their faecalme-tabolites. Four criteria had to be confirmed before this hypothesiscouldbetentativelyaccepted:(i)haresaresensitivetostresscaused

bypredation risk; (ii) increasedmaternal stress results inadecreaseinreproduction;(iii)maternalstressisinheritedfrommotherstooff-spring; and (iv)offspring fromstressedmothers alsoproduce feweroffspring.The first threeof thesepredictionshavebeenconfirmed.Breedingfemalesweremoststressedduringsummersofpeakpreda-tornumbers,stressedfemalesproducedfeweroffspringandtheoff-springofstressedfemalesalsowerealsostressed(Figure5),sothatthecontinuationofreproductivefailurewascarriedfromgenerationto generation bymaternal effects.We still need to show that highpredator-inducedstresscausesafailuretoproducelatesummerlitters3and4,andthatoffspringfromstressedmothersactuallyhavehighstresslevelswhentheythemselvesbreed.

The exact mechanism by which maternal stress programmesoffspring isnotyetknown. Itdoesnotappear tobedue togeneticchanges(Sinclair,Chitty,Stefan,&Krebs,2003).Changesingeneex-pressionhavebeen found (Lavergne,McGowan,Krebs,&Boonstra,2014) and themost plausible hypothesis is that these changes arelinked to epigenetic changes in expression of key regulatory genes,especiallythoseaffectingthestressaxis(Ho&Burggren,2010).Oneof the central enigmasof thehare cycle is the2–5-year lowphase

F IGURE  4 Snowshoehareautumnpopulationdensity(perha)oncontroltrappinggrids,1977–2016.Upper95%confidencelimitsareshown.Therehasbeenagradualbutslightlyunevendeclineinpeakdensitiessincethe1981peak[Colourfigurecanbeviewedatwileyonlinelibrary.com] 1980 1985 1990 1995 2000 2005 2010 2015

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following the decline (Figure4). If there is stress-induced maternalprogrammingofoffspringthatpersistsintoadulthood,thiscouldex-plainthelowphase.Butwhydoesitlastavariablelengthoftimeandwhatcauses the femaleseventually to return to theirhighly fecundstate?Wesuspect,butdonotknow,thattheepigeneticchangesmaytake time todiluteoutof thepopulation.Sheriff,McMahon,Krebs,andBoonstra (2015) found that the lengthof the lowphasewas afunctionoftheseverityofthedeclinephase,suggestingthatthemoreseverethepredationrisk,thegreatertheepigeneticsignature,andbyextension, themore generations required to remove that signature.Thisworkinghypothesisremainstobetested.Analternativehypoth-esisbyTyson,Haines,andHodges(2010)suggeststhattheprolongedlowphaseofthecyclemaybeduetothespecialrolethatgreathornedowlsmayplayaspredatorsduringthisphase.Thecyclelowandthefactorsthattriggerthereturntoincreaseremaintheleastwell-studiedcomponentsoftheharecycle.

2.2.5 | Alternative hypotheses for the decline in survival rates

Therearemanypredatorsthatfeedonsnowshoeharesfrom“herbi-vores”likeredsquirrels(Tamiasciurus hudsonicus(Erxleben))andgriz-zlybears(Ursus arctos(L.))tomorespecializedcarnivoreslikeCanadalynx(Figure6).Theresultofthisfoodwebisthatfewharesdieofoldage,andforabout95%ofharestheimmediatecauseofdeathispre-dation(Boutinetal.,1986;Hodgesetal.,2001).Butthecycleisoftenmislabelledandmodelledasahare–lynxcycle,andthereisaneedtoconsidermodelsthatconsidermultiplepredatorsaswellasmultiplepreyspecies(Tysonetal.,2010).

Twoalternativeexplanationsfordeclinesinharesurvivalarethatparasitesordiseasesreducetheconditionofhares,thusallowingpred-atorstodeliverthecoupdegrâce.Thereisasyetnogoodevidencethat this explanation operates in the Kluane system (Sovell, 1993).

Keith,Cary,Yuill,andKeith(1985),Keith,Keith,andCary(1986)car-riedoutanextensivestudyofhelminthparasitesofsnowshoeharesin centralAlberta.Fiveparasite specieswereprominent in theharepopulationbuttherewasnoindicationthatprevalenceaffectedanyreproductiveparametersoftheharepopulationoverthepopulationcycle.Murray,Cary,andKeith (1997)reducednematodeprevalenceexperimentally inharesduring2yearstodetermine ifparasitism in-creasedvulnerabilitytopredation.Virtuallyallharesintheirstudydiedfrompredation,andtheyfoundasignificantincreaseinpredationonuntreatedharesrelativetotreatedones,whichsuggestedthattheremightbeaninteractionbetweenparasitismandpredation.

IntheKluaneareatherehasbeennoevidencefoundofhighmor-tality insnowshoeharesdirectly fromdiseasesorparasitism,sotheonlypotential linkmaybethrough increasingvulnerabilitytopreda-tors.Theroleofpathogensinthesystemisasyetunexplored.Moreresearch is needed on the role of parasites and pathogens in harecycles,althoughourKluanestudieswouldsuggestthattheseeffectswouldbesmall.Inthesamemanner,weandotherslikeMurrayetal.(1997)havefoundalmostnodeathsinharesthatcouldbeascribedtostarvation(Hodgesetal.,2006).Harepopulationsdeclineinthepres-enceofsuperabundantfood,asshowninFigure1.

2.2.6 | Synchrony in snowshoe hare cycles

ThereremainsawidespreadbeliefthatsnowshoeharecyclesoccurinsynchronyacrossallNorthAmerica.Thisisnotcorrect,aswaspointedout longagobyChitty (1950).Thereality ismuchmore interesting.Smith(1983)analysedthequestionnairedataoftheSnowshoeRabbitEnquiryofthe1930sand1940sandsuggestedthatharepeaksfol-lowedatravellingwave(Figure7)withdelaysupto4years inpeaknumbersacrossCanada.

Todetermineifatravellingwaveiscurrentlyoccurring,Krebsetal.(2013) gathered the existing survey data of snowshoe hares from

F IGURE  6 HerbivoreandcarnivorefoodwebformajorspeciesintheKluaneYukonterrestrialecosystem.Speciesshadedinyellowarethemainspeciesforwhichwehavequantitativedata.Occasionaldietitemsarenotshowninthisdiagram[Colourfigurecanbeviewedatwileyonlinelibrary.com]

Snowshoehare

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Weasel

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central British Columbia, Yukon, Northwest Territories and Alaskafrom1970to2012.NoextensivedatawereavailablefromcentralandeasternCanada.ThewesternpartofthetravellingwavedescribedbySmith(1983)fromtrapperquestionnairedatainthe1930sand1940sstillexists(Figure8).Thereasonforthistravellingwaveisnotyetclear.Thebestsuggestionisthatitresultsfromthemovementsofsurpluspredators insearchofhigherpreyabundanceasthesnowshoeharepopulationcollapses(Sherratt,2001).Weknowfromcollaredanimalsthatlynxmoveinalldirectionsupto1100kmfromtheirpointoforigi-nalcapture(Mowat,Poole,&O’Donoghue,2000)(Figure9).Rowetal.(2012)showedthatCanadalynxwereessentiallypanmicticacrossall6000kmoftheCanadianmainland,suggestingwidespreaddispersalonacontinentalscale.

If patterns of synchrony are indeed driven bymobile predators,wearestill leftwithneedinganexplanationofwhythecycleseemsto“start”incentralSaskatchewanandradiateoutwards(Figure8).Wehavenoideawhythismightbe.

2.2.7 | Variable amplitude in snowshoe hare cycles

Afinalgeneralobservationabout10-yearcycleshasbeenthattheyarehighlyvariableinamplitude(Krebsetal.,2014).Someharepeaksare very high (super-peaks) and show obvious signs of extensivebrowsingonwintershrubs,andotherpeaksarenearlyinvisibletothecasualobserver (Figure4).Understanding theproblemofamplitudevariationisalandscapeissuewithalltheproblemsofstudyingeventsthatarespatiallyextensive (Lewis,Hodges,Koehler,&Mills,2011).Onasmallscale,GinzburgandKrebs(2015)exploredthepossibilitythatsnowshoeharecycleamplitudewasdefinedbytheminimalabun-danceofharepredatorsinthelowphaseofthecycle.Becauseallthepredatorsofharesincreasemoreslowlythanhares,hareswillescapeheavypredationlossesforalongerphaseofincrease,thusreachinghigher densities until thepredators catchup.Hence, the lower thedensityofpredatorsduringthelowphase,thegreaterthepeakharedensity and themore browsing damage. This hypothesisworks for

F IGURE  7 SynchronyinsnowshoeharecyclesacrossCanadafrom1931–1948,asmeasuredbyquestionnaires(Chitty,1950).TheaveragepeakphaseacrossCanadawasscaledas0.0,andthecontourlinesindicatepeaksoccurringearlierthanaverage(red,negativecontours)orlaterthanaverage(green,positivecontours).DuringthisperiodharepeakswerereachedearliestinthecentralborealregionofnorthernSaskatchewanandManitoba(AfterSmith,1983)

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Kluaneharepopulationsbutneedstobetestedinotherpartsofthehare’sgeographicrange.

Theeffect of habitat patchinessonhare cyclic amplitudeoffersanotherexplanationofsuper-peaks.Extensiveforestfires,forexam-ple,mayproduceoptimalharehabitatoverlargeareas.Ifwhatisopti-malforharesismuchlessoptimalforpredators,thiscouldaffecttheoverallpredationpressureduringthepopulationincreasephase.Inasimilarmannerifparasitesvaryinabundanceinareasfragmentedbyfires,areductioninparasiteprevalencemightallowbetterreproduc-tivesuccessandsurvival(Murrayetal.,1998).

2.2.8 | Hare cycles in eastern North America and eastern Eurasia

AllouractivitieshavebeenfocusedinwesternNorthAmericaandwedonotknowthedegreetowhichtheyapply totheboreal forestofeasternNorthAmerica,butweexpectthattheydo.The10-yearcycleisdominantintheborealforestofCanadaandacrossSiberiabutintheboreal forestof northernEurope3–4-year cyclesofvolesdominatecommunity processes. Boonstra etal. (2016) explained these strik-ingdifferencesasbeingclimaticallydriven (Figure10).Temperaturesin the formerare15–20°Ccolder inwinter.Thisdirectlyaffects thevegetationthatcanoccuronthetwoareas—tallshrubs(birchandwil-low)areadaptedtoseverecoldandshallowsnowsofwinteranddomi-nateinwesternNorthAmerica,whereasaluxuriousdwarfshrublayer

(Vacciniumspp.)isadaptedtothemildtemperaturesanddeepsnowsanddominatesinnorthwesternEurasia.Ultimatelytheoccurrenceofthe10-yearcycleintheborealforestofNorthAmericaisdrivenbot-tom-upbyseverewinterclimate.Thatbeingthecase,wepredictthatseverityof thewinterclimatewillmaintain the tall shrubvegetationasoneprogresseseastwardacrossthecontinent(hencethedecliningtreelineasoneprogresseseastward)andthat10-yearcyclesareex-pectedtooccurthroughouttheseborealforestregions.InEurasia,thewesternregionsareheavilyinfluencedbywarmairmassesandmari-timeclimatefromtheAtlantic.However,eastoftheUralMountains,weexpectaseverecontinentalclimate(analogoustothatinnorthernCanada)acrossSiberiaandwithitachangeinthevegetationtofavourtallshrubsintheunderstoreyand10-yearharecycles.Theevidence,basedonfur returnsover relativelyshort timeperiodsof~20years,issuggestive,butconsistentwiththisprediction.Bulmer(1984)con-cluded that the mountain hare appeared to have a cycle length of8yearsintheKomiregionjustwestoftheUrals,andof11yearsinthefareastofSiberiaintheYakutiaregion.Inbothcases,thepeakintheEuropeanlynxreturnslagged1–2yearsbehindtheharepeak.

2.3 | Models of the hare cycle and alternative approaches

Turchin(2003)formulatedseveralcriticismsofourexperimentalwork,the most notable being that our predictions and analyses were not

F IGURE  8 AtravellingwaveofpeaksnowshoehareabundanceinnorthwesternNorthAmericaduringtheperiodfrom1970to2012.Reddotsindicatesiteswithquantitativedataonhareabundance.Bluearrowsindicateapproximatetravellingwavewitheachadditionalarrowfromsouthtonorthindicatinga1–2yeartime-laginthearrivalofpeaknumbers(DatafromKrebsetal.,2013)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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theoretically informedbyanysortofmathematicalmodel;somethingheconsideredtobeessentialwhendealingwithsystemsdrivenbycom-plexnonlineardynamics.Theessenceoftheargumentiscapturedby

KingandSchaffer(2001)whentheystatethat“qualitativedifferencesinbehaviourcanresultfromquantitativedifferencesinparametervalues”such that “the articulationof alternative verbal hypotheses and their

F IGURE  9 DispersalmovementsrecordedfromradiocollaredCanadalynxfromthepointofcaptureintheYukonandNorthwestTerritoriestothepointofdeathduetofurtrapping.Amaximumstraightlinemovementof1,100kmhasbeenrecorded(AfterMowatetal.,2000)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

F IGURE  10 Aproposedexplanationforhowwinterclimate—actingmainlythroughtemperatureandsnowquantity—giverisetothedifferentvegetationandfoodwebdynamicsfoundintheborealforestsofwesternNorthAmericaandnorthwesternEurope(FromBoonstraetal.,2016)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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evaluationbystronginference—theconventionalbiologicalapproach—maybedoomedfromtheoutset”.Weinterpretthistomeanthatde-pendingoncircumstances,ourexperimentaltreatmentsmightpointtotheimportanceofonefactor,whereasinanothercycletheycouldpointtoanalternativefactoreventhoughtheunderlyingmechanismsforthecycleremainconsistent.Theonlywaytoevaluatethisargumentiswithreplicatedstudiesondifferentharecycles.Thishasbeendonenowfor45yearsatKluaneLakeandourworkwasbasedonpioneeringexperi-mentsandstudiesbyLloydKeithandhiscolleaguesinAlberta(Keithetal.,1984).Theresultofthesereplicatestudiesisthatthedemographyandproximatecausesofmortalityofthecyclesstudiedareconsistent,sothatasinglesetofmechanismsshouldbesoughtasanexplanation.

Attempts to model the hare cycle have been surprisingly few(summarizedinKorpimäki&Krebs,1996).EarlymodelspublishedbyFoxandBryant(1984)andTrostel,Sinclair,Walters,andKrebs(1987)servedasbackground forourexperimentalmanipulations,but largegaps in the empirical informationneeded to parameterize the sortsofmodelssuggestedbyTurchin (2003) limitedtheirutility.KingandSchaffer(2001)constructedastandardtrophicinteractionmodellink-ingvegetation, hares and predators (Turchin, 2003) and parameter-ized itusing theempirical findings fromRochester andKluane.ThemodelcouldproducecyclesthatweresimilarinperiodandamplitudetoempiricalobservationsanditwasalsoabletoreproduceresultsoftheKluaneexperiments.KingandSchaffer(2001)analysesledthemto the following conclusion: “Regardless of the relative importanceofpredationandstarvationinagivenlocale,themodelpredictsthatalthoughresource limitation isresponsibleforarrestingthe increasephase of the cycle, it is increasing predation mortality that bringsaboutthecrash.”TheKingandSchaffermodelhasbeencriticizedasbeing“overfitted”becauseofthelargenumberofparametersinvolved(Ginzburg&Jensen,2004). Inaddition, thekey linktovegetation inthemodelwascreatedbyastandarddensitydependencerelationshipbetweenhareconditionandreproductionormortality.Therewasnoconsiderationofthenon-consumptiveeffectsofpredationonharere-productionhypothesizedbyBoonstraetal.(1998)asanalternativetoresourcelimitationasanexplanationofreproductivechanges.

Allinall,empiricalstudiesandmathematicalmodelsareimportanttoolsfortestingfactorsimportantintheharecycle.WedonotagreewithTurchin(2003)thatsystemsshouldbemodelledbeforeproceed-ingwith empirical studies and experiments. Bothmethods need toinformtheother.Wehavebeenfrustratedbythelackoftestablepre-dictionsstemmingfrommodellingpapers(butseeKingandShafferforanexception)andwehavepointedoutsomeofthefrustrationsmod-ellershavewithourempiricalanalyses.Intheend,theconclusionsofthemodellingworkwerenotvastlydifferentfromourempiricalworkor the statisticalmodelling of Stenseth, Falck, Bjørnstad, andKrebs(1997)butmorelinkagebetweenvariousapproachesisneeded.

3  | DISCUSSION

Whenthe10-yearcycleofsnowshoehareswasfirstdescribedabout100years ago by biologists, therewere amultitude of hypotheses

suggested aboutwhat the cause of these cycles could be. The listofpossiblemechanisms forpopulation changes is very large, start-ing with climate, food supplies, predation, parasitism, disease andan array of social factors like territoriality and infanticide. Each ofthesegeneralmechanismscanthenbebrokendownintoaseriesofalternatives.Forexample,foodshortageasageneral limitingfactorcouldoperateinsummerorwinter,involvejuvenilesoradults,couldinvolve foodquality aswell as quantity, andbe involvedwith sec-ondarychemicals in the foodplants. Ifwetakeonly the fivebroadcategories above,we can calculate that there are31 combinationsofthese,eachoneofwhichisadistincthypothesis.Facedwiththisimpossibleagenda,ecologistsmustusenaturalhistoryinsightstore-ducethehypothesestoamanageable level.Giventhisreduction inpossiblemechanisms,wemust testeachhypothesisexperimentallyinthefield.Wehavefocusedonfoodandpredationasthetwomostlikelymainprocessesdrivingharepopulationdynamics.Sinceinthiscase eachexperimental testmust be carriedout for10years, pro-gresscannotberapid.

There are two shortcuts to do this difficult, bottom-up exper-imental work. First, one could build a mathematical model of thecycle and compute the consequences of the assumptionsmade inthemodel.This isanattractive top-downmethodologybut, inourcase,despiteextensivemodellingbymanyecologists,littlelightwasshedon theactualmechanisms causing the cycleuntilwedidourmanipulationsatKluaneLake.Thereasonforthis istwofold.Manymodelscontainparametersthatcannotpossiblybemeasuredinnat-uralsystems.Secondly,awholehostofsimplifyingassumptionsmustbemade to avoid an infinite regress inmodel building.The resulthasbeenthatahostofmodelsexistforcyclicpopulationdynamics,virtuallynoneofwhichareusefulinguidingexperimentalstudiesinnaturalsystems.

Asecondshortcut inecologicalstudieshasbeentoutilizelab-oratorypopulationsinmicrocosmstomimicnature.Whilethisisausefulstrategyformanysystems, itdoesnotworkformammalorbirdpopulationsbothbecauseofscaleandoflackofcomplexityandrealism.The dispersal of individuals is a critical process formanypopulations, and in every moderate size microcosm it is difficulttopermitdispersaldynamicsandhabitatselectionaswouldoccurinnaturalecosystems.Homerangesofsnowshoeharesvary fromabout2hato7hadependingonsexanddensity(Boutin,1984),sothatholdingharesinsmallenclosuresriskspotentialartefacts.Themostmisleadingearlyepisodeforsnowshoehareswastheconclu-sionofGreenetal.(1939)thatshockdiseasecausedharedeclines(Chitty,1959).

Boththefoodandthepredatorhypothesesaredifficulttotestforfieldpopulationsunlessclearhypothesesarestatedwithexplicitpre-dictionsandunlessexperimentalmanipulationsarecarriedout.Thisisperhapsthemajoradvanceofourworkoverthelast40years—thatexperimental design is critical for population studies andmanipula-tionscanbedoneatrelevantspatialscales.Buttheothercrucialthinghereisthatwehadtolookinsidetheblackboxthatistheanimaltolookformechanismsthatmightexplainthereproductivechanges intheharecyclefromstudiesofstressphysiology.

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3.1 | Next steps

Wenowhaveinformationintheliteratureonthreetofivecompletesnowshoeharecyclesfromonlytwostudyareasintheborealforest.Todate,thebasicpatternsseemconsistent;predationisaprimedriverofthecycle,buttherearefourimportantareasforfutureresearch.

1. The Kluane experiments need to be repeated and improvedupon. There is a clear need for geographic expansion of studiesto other regions of the boreal forest and further replication.

2. Themechanismbehind thedecrease inhare reproduction in thelate increase,peakandcrashneeds tobepreciselynaileddown.Thecurrenthypothesisofan indirect,non-consumptiveeffectofpredationviathestressaxisneedsfurthertesting.

3. Thecycliclowandearlyrecoveryremainsasthemostpoorlyun-derstoodpartofthecycle.At leasttwohypothesesnowexisttoexplainthelowphaseandmodelscouldbeusefulintestingideasas

tothemagnitudeandmechanismofhowmaternaleffectscouldactanddisappearduringthelow.

4. Newtechnologieslikeproximityradiocollarsareavailabletofollowthespatial locationandactivityofharesandtheirpredators,andshouldprovidebetterinsightintoboththeconsumptiveandnon-consumptiveeffectsofpredatorsonharedemography.

4  | CONCLUSIONS

The early knowledge of snowshoe hare cycles helped tomove thescientificconsensusawayfromtheideathatnaturewasinastateofbalance,whichwasdisturbedonlybyhumansorperhapsangrydei-ties.Ittookecologistsuntilabout1950tobegintotakeseriouslythequestionofwhynaturalpopulations fluctuated,andwhatwecoulddo about them if they damaged our livelihoods. Snowshoe hares

F IGURE  11 Flowchartofthe40yearsofresearchthathaveallowedustodevelopacomprehensiveviewoftheecologicalmechanismsbehindthe10-yearcycleofsnowshoeharesintheYukon.Thenegativesymbolsindicatenoeffectoftheproposedfactor[Colourfigurecanbeviewedatwileyonlinelibrary.com]

Does winter food shortage cause the hare cycle?

Do predation and food shortage together cause the hare cycle?

HypothesisConfirmation

Is stress level inherited?

Measure stress in reproductive females

over the cycle

Predation causes the hare cycle both via direct mortality and reduced reproduction. Predator chases stress females,

resulting in a reduction in reproductive output. Stress effects are inherited via a maternal effect, which maintains a

low phase for 2–4 years.

Manipulate winter food

Interactive effects of added food and predator reduction

Manipulate summer and winter food and reduce predation and combine these treatments

Does food shortage cause reduced reproductive output?

Could predators cause reduced reproductive output?

Measure stress in offspring of stressed

females

98  |    Journal of Animal Ecology KREBS Et al.

were an early bellwether of ecosystem fluctuations that needed tobeunderstoodinnorthernlandscapes.Assuchtheybecameaclassi-calCanadianecologicaliconthatappearsinthebeginningofalmosteverybiologytextbook.

Wehaveachievedatentativeexplanationofwhatcausessnow-shoe hare cycles (Figure11). That is progress in our view. But werecognizethatallscientificconclusionsaretentativenomatterhowextensive the study. In our case,wedraw the sweeping conclusionthat thecauseofsnowshoeharepopulationcyclesacrossallof theborealforestsofCanada,AlaskaandSiberiaarecausedbypredationactingdirectlyonmortalityandindirectlyonalandscapeoffearpro-ducing chronic stress in breeding females.We have no idea if thissweeping generalization is correct, and can onlywait for additionalstudiesofhares across thisvast region to testour conclusions.Wefully subscribe to the conceptof scienceas “conjectureand refuta-tion,”andthereisstillmuchtodototestourunderstandingofborealforestecology.

We have gradually expanded ourview from population ecologytocommunityandecosystemecologyoftheYukonborealforest.Theinteractionsbetweenthecomponentsoftheborealforestcommunityneedtobedescribedandunderstoodbeforewecanhopetopredicthowclimate changewill alter these interactions.Wewould suggestthatdetailedstudiesofmovementpatternsofthemajorpredators—coyotes (Canis latransSay), lynx,greathornedowls (Bubo virginianus Gmelin)andgoshawks(Acciper gentilisL.)—inthisecosystemwillhelpus to tiewhat happens locally to the extensive forests of northernNorthAmerica.Thereisamajorgapinthefewcurrentstudiesofplantdynamicswithinthisecosystem,bothfromthepointofviewofplant–herbivore interactionsand thatofplant successionduringa timeofrapidclimatechange.Theseissuesarelong-termproblemswithwhichsciencedealspoorly. Ifunderstanding theharecyclewasa40-yearproblem,withmanyquestionsyet unanswered, the community andecosystemissuesintheborealforestare100-and200-yearproblemsatatimewhenthesciencefundingtimeframeis3–5years.Weneedto askourselveswhat theecologistsof theyear2100willwishwehaddonenowtoadvancetheunderstandingofnaturalsystems.Afairquestionwithnosimpleanswer.

ACKNOWLEDGEMENTS

This researchwouldnot havebeenpossiblewithout the collabora-tionofmanyuniversity professors, graduate students, postdoctoralfellowsandtechnicians.Inparticular,wethankTonySinclair,thelateJamieSmith,RoyTurkington,KathyMartin,SusanHannonandMarkDalefortheircollaborationonthemajorproject.AliceKenneyisthelongestservingresearchassociate,followedcloselybyIreneWingate,Scott Gilbert, Jean Carey, Elizabeth Hofer, Peter Upton and MarkO’Donoghue.Manyofourresearchstudentsandassistantshavegoneontofurtherresearchpositions,includingDavidHik,KarenHodges,DennisMurray,VilisNams,MichaelSheriff,JeanCareyandRichardWard. For all our summer assistants and volunteers, we are mostgrateful for thehelp thatallowedus toachieveour researchgoals.FundingforthisresearchprojectwasprovidedbytheNaturalSciences

and Engineering Research Council of Canada. The authors declarenoconflictofinterestinthispublication.ThefacilitiesoftheKluaneLakeResearchStationoftheArcticInstituteofNorthAmericawere essentialtothislong-termresearchprogramme,andwethankAndyandCaroleWilliamsandSianWilliamsandLanceGoodwinfortheirassistance.WededicatethisreviewtothememoryofCharlesEltonandDennisandHelenChittywhopioneeredallthisresearch.

AUTHORS’ CONTRIBUTIONS

Allauthorscontributedtothefieldresearchandtothewritingofthissynthesispaper.

DATA ACCESSIBILITY

Thesnowshoeharepopulationdatapresentedhereareavailablefromthe Dryad Digital Repository https://doi.org/10.5061/dryad.684s1(Krebs,Boonstra,&Boutin,2017).Thesedataincludethemetadata,phasesofthepopulationcycle,capture–recapturedataforallthecon-trolgrids live trapped, fence+foodmark–recapturedata,populationestimatesforcontrolgridsandforthenaturalfeedingexperiment.

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How to cite this article:KrebsCJ,BoonstraR,BoutinS.Usingexperimentationtounderstandthe10-yearsnowshoeharecycleintheborealforestofNorthAmerica.J Anim Ecol. 2018;87:87–100. https://doi.org/10.1111/1365-2656.12720