Do bees matter to cranberry? By · will forever appreciate your patience, dedication, and...

Do bees matter to cranberry?

The effect of bees, landscape, and local management on cranberry yield

Hannah Rodman Gaines Day

A dissertation submitted in partial fulfillment of

the requirements for the degree of

Doctor of Philosophy

(Zoology)

at the

UNIVERSITY OF WISCONSIN‐MADISON

Date of final oral examination: 10/09/13 The dissertation is approved by the following members of the Final Oral Committee: Claudio Gratton, Professor, Entomology Russ Groves, Associate Professor, Entomology Shawn Steffan, Assistant Professor, Entomology Volker Radeloff, Professor, Forest and Wildlife Ecology Neal Williams, Associate Professor, Entomology (University of California, Davis)

TABLEOFCONTENTSDEDICATION……………………………………………………………………………………………………………...…iiiACKNOWLEDGEMENTS………………………………………………………………………………………………..ivTHESISABSTRACT…………………………………………………………………………………………………….....viTHESISINTRODUCTION……………………………………………………………………………………………..…1CHAPTER1:Non‐bioticfactorscontributetocranberrypollination Abstract………………………………………………………………………………………………………………7

Introduction………………………………………………………………………………………………………..8

Methods…………………………………………………………………………………………………………….11

Results………………………………………………………………………………………………………………16

Discussion…………………………………………………………………………………………………………18

Literaturecited…………………………………………………………………………………………………..23

Figures………………………………………………………………………………………………………………27

Appendix…………………………………………………………………………………………………………...31

CHAPTER2:Thecontributionofhoneybeestocranberryyieldvarieswiththeamountofwoodlandinthesurroundinglandscape Abstract……………………………………………………………………………………………………………..36

Introduction………………………………………………………………………………………………………38

Methods…………………………………………………………………………………………………………….40

Results………………………………………………………………………………………………………………42

Discussion………………………………………………………………………………………………………….44

Figures………………………………………………………………………………………………………………51

CHAPTER3:Localandlandscapefactorsinfluencenativebees,yield,andthecontributionofbeestoyield Abstract……………………………………………………………………………………………………………..54

Introduction………………………………………………………………………………………………………55

Methods…………………………………………………………………………………………………………….58

Results………………………………………………………………………………………………………………64

Discussion………………………………………………………………………………………………………….67

Figures………………………………………………………………………………………………………………76

Appendix…………………………………………………………………………………………………………...84

CHAPTER4:Understandingthebarrierstoimplementationofon‐farmhabitatconservationofnativebeesinWisconsincranberry Abstract……………………………………………………………………………………………………………..89

Introduction………………………………………………………………………………………………………90

Methods…………………………………………………………………………………………………………….93

Results………………………………………………………………………………………………………………95

Discussion………………………………………………………………………………………………………..100

Literaturecited………………………………………………………………………………………………..104

Figures…………………………………………………………………………………………………………….108

Appendix…………………………………………………………………………………………………………117

THESISCONCLUSION………………………………………………………………………………………………...129

Formybuddyoldpal,Becky.Myfirstentomologyteacherandagreatfriend.

Thisoneisforyou.

ACKNOWLEDGEMENTS Therearemanypeoplewhohavehelpedandguidedmethroughoutmygraduate

schoolcareerbutnoneasmuchasmyadvisor,ClaudioGratton.UnderClaudio’sguidanceI

havebecomeabettercommunicatorandscientist.Icannotimagineabetteradvisor,

teacher,androlemodel.Thankyou,Claudio,forbeingawesome.YouaretrulygreatandI

willforeverappreciateyourpatience,dedication,andenthusiasm.Iamalsogratefultothe

cranberrygrowerswhoallowedmetoconductmyresearchontheirmarshes.Iam

humbledbytheirgenerosityandkindness.IamespeciallygratefultoC.J.SearlesCranberry

forallowingmetoconductmyintensivefieldstudyontheirmarshandGaynorCranberry

Inc.forallowingmetodigcranberryplantsoutoftheirmarshformygreenhousestudy.

Iwouldalsoliketothankmycommitteemembers,VolkerRadeloff,NealWilliams,

RussGroves,andShawnSteffanfortheircontinuedsupportandfeedbackthroughoutmy

PhD.IalsothankPaulMitchellforhisenthusiastichelpwithmyhoneybeechapter.I

wouldliketothankthemembersoftheGrattonLabfortheirhelpwithdatacollection,

statisticalanalysis,andgeneralfeedback,especiallyRachelMallinger,TaniaKim,Brian

Spiesman,andDavidHoekman.IwouldalsoliketothankDavidDuncanforhelpwith

statisticalanalysis.Thecranberryresearchgroup,especiallyEricZeldinandBeth

Workmaster,providedvaluablefeedbackonfieldandgreenhouseexperiments.John

Ascher,MikeArduser,andJasonGibbsspentmanyhoursidentifyingandverifyingmy

nearly10,000beespecimens.DanCariveauwasasoundingboardthroughoutmy

dissertationandprovidedvaluablefeedbackonearlydrafts.IwouldliketothankBritt

SearlesandtheSandhiltonforprovidingaplaceformetostayduringmyfieldwork.Jayne

SojkaandDanMahrhelpedwithmyinitialfieldsiteselectionandprovidedcontinued

supportthroughoutmyPhD.

Iamalsogratefultothefieldandlabassistantswhohelpedmecollectandprocess

mydataespeciallyCollinSchwantesandAmandaRudiewhostuckwithmethrough18

hourfielddays,blisteringheat,numbingcold,wind,rain,anddarknesstogetthedata

collected.Theirdedicationandeffortwasremarkable.IalsothankEmilyFricke,Adam

Higgins,CarlKaiser,LauraSmith,MerrittSingleton,AllisonDehnel,BrianHedberg,Chase

Fritz,MollyWaytes,GavinJones,FedericaLacasella,JuliaTiede,AliNelson,Alex

Wenninger,CaitlinBergstrom,EricWiesman,ChristopherWatson,SachaHorn,andScott

Leefortheirhelpinthefieldandlab.

Icouldn’thavefinishedmydissertationwithouttheweeklyaccountabilitymeetings

withAlexLyon,MarySaunders,andDavidDuncan.Iamalsogratefultothefolksatthe

WritingCenterforprovidingstructureandwritingadvicethroughoutthewritingprocess.

IamgratefultoKatharinaUllmannandMiaParkforbeinggreatfriendsandgiving

meadviceonfieldworkandresearch.

Andfinally,Iamgratefultomyfamily,friends,andmyhusband,Steve,for

supportingme,lovingme,andenrichingmylife.Icouldn’thavedoneitwithoutyou.

THESISABSTRACT

Nativebeesprovidethemajorityofpollinationservicestowildandcultivated

floweringplants.Unfortunately,astheareaofmodernagricultureexpands,fragmenting

anddestroyingnaturalhabitat,thepersistenceofnativebeesandthepollinationservices

theyprovideisthreatened.Withthecurrentdeclineinmanagedbees,understandinghow

localmanagementdecisionsandlandscapefactorsinfluencenativebeesandtheir

contributiontocroppollinationbecomesmoreurgent.UsingWisconsincranberryasa

modelsystem,Iexaminedthepollinationrequirementsofcranberry,thecontributionof

beestopollination,andtheinfluenceoflocalandlandscapefactorsonnativebees.I

furtherinvestigatedthebarrierstofarmeradoptionofon‐farmconservationprogramsfor

nativebees.Contrarytopreviousstudies,Ifoundthatnon‐bioticfactorscontribute

significantlytocranberrypollination(chapter1).Myresearchdemonstratesthat,evenin

theabsenceofbees,cranberryisabletoproducefruit.Fruitproductionwas,however,

increasedwhenbeeswerepresentsupportingthepracticeofusinghoneybeesfor

pollination.Atafarmscale,cranberryyieldwaspositivelycorrelatedwithanincreasing

stockingdensityofhoneybeehives,butonlyatfarmslocatedinlow‐woodlandlandscapes

(chapter2).Whenhoneybeeswereabsent,allfarmshadsignificantyield,butthoseinhigh

woodlandlandscapeshadamarginallyhigheryieldthanfarmsinlowwoodland

landscapes.Farmsinhighwoodlandlandscapesalsohadahigherabundanceandrichness

ofnativebeesalthoughtherewasonlyaweakrelationshipbetweennativebeesandyield

(chapter3).Thecontributionofbeestocranberrypollinationincreasedwithincreasing

floweringuprightdensity,suggestingthatlocalmanagementcanenhancethecontribution

bybees.Additionalresultsindicatethatcranberrygrowersareinterestedincreating

pollinatorhabitatontheirfarmsbutarelimitedbyalackoftechnicalsupportand

perceivedtimeandfinancialcommitments(chapter4).Thisdissertationcontributesto

ourunderstandingofcranberrypollinationbiologyandhowlocalandlandscapefactors

influencebeesandtheircontributiontoyield.Iprovidepracticalguidelinesforgrowerson

pollinationmanagementforcranberryandforconservationprofessionalsonincreasing

cranberrygrowerparticipationinfederalpollinatorconservationprograms.

THESISINTRODUCTION

Theexpansionofmodernagricultureandhumanactivityhasledtothealteration

andfragmentationofthelandscape(Vitouseketal.1997,Foleyetal.2005).Theresulting

lossofhabitathasprofoundeffectsontheabilityoforganismstopersist(reviewedby

Fahrig2003)andtheprovisioningofecosystemservices(Lucketal.2003).Theresponse

ofspeciesthatdirectlyinfluenceecosystemservicessuchaspollinationisofparticular

importance.Insect‐derivedecosystemservicesaloneareworthanestimated$8billionper

yearanddirectlyimpacthumanwellbeing(LoseyandVaughan2006,Eilersetal.2011).

Pollinationisaparticularlyimportantserviceinagro‐ecosystemsasitisrequiredby

orbenefitstwo‐thirdsofglobalcrops(Kleinetal.2007).Ashoneybeescontinuetodecline

(Ellisetal.2010),farmersmayneedtoseekalternativewaystopollinatetheircrops.

Nativebeesprovidevaluablecroppollinationservices(LoseyandVaughan2006,Winfree

etal.2008)butareatriskofdeclineduetohabitatlossandfragmentation,intensified

agriculture,andagri‐chemicalexposure(Pottsetal.2010).Sincebeesarecentralplace

foragersandhavelimitedflightdistances(Greenleafetal.2007,Zurbuchenetal.2010),

theyrequirereadilyaccessiblenestingandforagingresourcesthroughouttheirentireflight

season.Becauseofagriculturalpracticesthatdisturbthesoil(e.g.,tilling),limitthe

abundanceoffloweringweedyspecies(e.g.,useofherbicides),andcultivatecropsas

monocultures,modernagriculturallandscapesprovidepoorhabitatforbees.

Onewayforfarmerstolessentheeffectsofmodernagriculturalpracticesonbeesis

throughtheadoptionofon‐farmhabitatconservationprograms.Providinghabitatwithin

agriculturallandscapescouldgreatlyenhancelocalresourceavailabilityandtheabilityof

beestopersistandprovidepollinationserviceswithincropfields.Cost‐shareconservation

programsthroughtheUnitedStatesDepartmentofAgricultureNaturalResources

ConservationService(USDANRCS)providegrowerswithfinancialincentivestoinstall

pollinatorhabitat.Inaddition,forfarmersofpollinator‐dependentcrops,suchas

cranberries,theadoptionoftheseprogramscouldprovideadirecteconomicreturninthe

formofincreasedpollinationservicesfromnativebees.Inorderforthisstrategytobe

successful,however,growersmustadoptthesepractices.Becauseoftheirdependenceon

pollinators,demonstratedcommitmenttoenvironmentalstewardshipthroughthe

adoptionofIntegratedPestManagement(IPM)programs,andtheavailabilityofnon‐crop

habitatontheirfarms,cranberrygrowersshouldbeidealcandidatesforadoptionof

federalon‐farmconservationprograms(ColquhounandJohnson2010).

Beforewecandeterminethesignificanceofpollinatordeclinetocropproduction,

however,weneedtounderstandthepollinationrequirementsofthecropanddetermine

howmuchbeescontributetoitspollination.Therefore,theobjectiveofthisstudywasto

gainabetterunderstandingofthefactorsthataffectpollinationandnativebeesinthe

Wisconsincranberrysystem.

Cranberryisgenerallyconsideredapollinator‐dependentcrop,althoughestimates

ofyieldlossintheabsenceofbeesvarygreatly(DelaplaneandMayer2000),suggesting

thatthepollinationrequirementsarenotclearlyunderstood.Therefore,inChapter1,I

designedcomplementaryfieldandgreenhouseexperimentstotestthecontributionofboth

bioticandnon‐bioticfactorstocranberrypollination.Iincludedtreatmentsforbiotic(i.e.

beeorbyhand),non‐biotic(i.e.agitation),andnopollination.Fromtheresultsofthese

studies,wewillgainabetterunderstandingofhowmuchpollinationcanbeattributedto

beesasopposedtonon‐bioticfactors.

ThemajorityofWisconsincranberrygrowersusehoneybeestomeettheir

pollinationrequirements,althoughtheoptimalhivestockingdensityisnotknown.While

therecommendedstockingdensityis2‐3hives/acre,actualmanagementrangesfrom0‐9

hives/acre.InChapter2,Iused11yearsofhistoricalyieldandhoneybeerecordsfrom

about40growerstodeterminetheeconomicallyoptimalstockingdensity.Theoptimal

stockingdensityisthepointatwhichanadditionalhiveresultsinnoadditionalincreasein

yield.Theresultsofthisresearchwillprovideanupdatedrecommendedhivestocking

densitythatcanbeusedbythegrowersfortheirpollinationmanagementpracticesinthe

future.

Anothersourceofbioticpollinationisnativebees.Inchapter3,Iinvestigatedthe

influenceoflocalfarmmanagement(i.e.,pesticideusage,plantuprightdensity)and

surroundinglandscapeonthesebees,aswellascranberryyield.Overthecourseofthree

fieldseasons,Ipantrappedbeesat49uniquesitesacrossalandscapegradient.In2011

and2012,Ialsocomparedyieldestimatesinopenplotsandpollinatorexclusioncagesto

determinewhetherlocalandlandscapefactorsinfluencethecontributionofbeestoyield.

Thischapterfurtheraddstotheliteratureontheeffectsoflocalandlandscapefactorson

nativepollinatorsandprovidesanewangleforlookingattheeffectofthesefactorsonthe

contributionofpollinatorstocropyield.

Whilewecanlearnalotaboutasystemthroughrigorousscientificstudies,

communicatingdirectlywiththepeoplewhomanagethesystemcanalsoprovidevaluable

insight.Ascientificstudytakesasnapshotofthesystem,butthegrowershavebeen

observingpatternsandactivityontheirfarmsforyearsandmayhaveamulti‐generational

perspectiveonmanagementdecisionsandoutcomes.Therefore,thefourthandfinal

chapterofmydissertationtakesasocialperspectiveoncranberrypollination,management

decisions,andon‐farmconservation.Thegoalofthischapterwastodeterminethe

barriersthatexistwhichpreventWisconsincranberrygrowersfromimplementingon‐

farmconservationprogramsfornativebees.Throughawrittensurveyofthegrowers,I

askedabouttheircurrentmanagementpractices,awarenessofnativepollinatorsand

pollinatorhabitat,andtheirattitudestowardandparticipationinon‐farmconservation

programs.Theresultsofthischapterwillprovideconcreterecommendationsforagency

personnelinordertotargetoutreachactivitiesandadjustprogramrequirementsto

increaseparticipationinUSDA–sponsoredon‐farmconservationprogramsfornativebees.

Fromthisresearch,wewillgainanunderstandingofthefactorsthatcontributeto

cranberrypollination,thevalueandoptimalstockingdensityofhoneybeesforcranberry

production,theinfluenceoflocalandlandscapefactorsonnativebeesandtheir

contributiontocranberryyield,andagrowerperspectiveonpollinationandon‐farm

conservation.Thisdissertationprovidestheresultsofrigorousscientificstudiesalong

withguidelinesforthepracticalapplicationoftheseresults.Itismyhopethattheresults

ofthisresearchwillbeusedbythescientific,grower,andagencycommunitiestoshape

furtherresearch,refinepollinationmanagementpractices,andimproveconservation

programstoincreasetheadoptionofon‐farmconservationfornativebeesinWisconsin

cranberry.

Literaturecited

Colquhoun,J.,andH.Johnson.2010.Sustainablecranberryproductionforavibrantfuture:TheWisconsinexperience.UniversityofWisconsin‐Extension.

Delaplane,K.S.,andD.F.Mayer.2000.Croppollinationbybees.CABIPublishing,New

York,NY.Eilers,E.J.,C.Kremen,S.SmithGreenleaf,A.K.Garber,andA.‐M.Klein.2011.Contribution

ofpollinator‐mediatedcropstonutrientsinthehumanfoodsupply.PLoSONE6:e21363.

Ellis,J.D.,J.D.Evans,andJ.Pettis.2010.Colonylosses,managedcolonypopulationdecline,

andColonyCollapseDisorderintheUnitedStates.JournalofApiculturalResearch49:134–136.

Fahrig,L.2003.Effectsofhabitatfragmentationonbiodiversity.AnnualReviewofEcology,

Evolution,andSystematics34:487–515.Foley,J.A.,R.DeFries,G.P.Asner,C.Barford,G.Bonan,S.R.Carpenter,F.S.Chapin,M.T.

Coe,G.C.Daily,H.K.Gibbs,andothers.2005.Globalconsequencesoflanduse.Science309:570.

Greenleaf,S.S.,N.M.Williams,R.Winfree,andC.Kremen.2007.Beeforagingrangesand

theirrelationshiptobodysize.Oecologia153:589–596.Klein,A.‐M.,B.E.Vaissière,J.H.Cane,I.Steffan‐Dewenter,S.A.Cunningham,C.Kremen,and

T.Tscharntke.2007.Importanceofpollinatorsinchanginglandscapesforworldcrops.ProceedingsoftheRoyalSocietyB:BiologicalSciences274:303–313.

Losey,J.E.,andM.Vaughan.2006.Theeconomicvalueofecologicalservicesprovidedby

insects.Bioscience56:311–323.Luck,G.W.,G.C.Daily,andP.R.Ehrlich.2003.Populationdiversityandecosystemservices.

TrendsinEcology&Evolution18:331–336.Potts,S.G.,J.C.Biesmeijer,C.Kremen,P.Neumann,O.Schweiger,andW.E.Kunin.2010.

Globalpollinatordeclines:trends,impactsanddrivers.TrendsinEcology&Evolution25:345–353.

Vitousek,P.M.,H.A.Mooney,J.Lubchenco,andJ.M.Melillo.1997.Humandominationof

Earth’secosystems.Science277:494.

Winfree,R.,N.M.Williams,H.Gaines,J.S.Ascher,andC.Kremen.2008.Wildbeepollinatorsprovidethemajorityofcropvisitationacrossland‐usegradientsinNewJerseyandPennsylvania,USA.JournalofAppliedEcology45:793–802.

Zurbuchen,A.,L.Landert,J.Klaiber,A.Müller,S.Hein,andS.Dorn.2010.Maximum

foragingrangesinsolitarybees:onlyfewindividualshavethecapabilitytocoverlongforagingdistances.BiologicalConservation143:669–676.

CHAPTER1

Bioticandnon‐bioticfactorscontributetocranberrypollination

Author:HannahR.GainesDay

Co‐author(s):ClaudioGratton

Forsubmissionto:JournalofPollinationEcologyorHortScience

Abstract:Asmanagedandnativebeepopulationscontinuetodecline,farmersface

possiblecropfailuresduetoinsufficientpollination.Crops,however,varyinthedegreeto

whichtheydependonpollinatorstomovepollenbetweenflowers,suggestingthatsome

cropsmaynotbeassensitivetovariationinpollinatoravailabilityorabundanceasothers.

Cranberry(Vacciniummacrocarpon)isgenerallyconsideredapollinator‐dependentcrop,

althoughestimatesofyieldlossintheabsenceofbeesvarygreatlyfrom30‐100%,raising

thepossibilitythatnon‐bioticfactorsmayalsobeimportantforcranberrypollination.The

objectiveofthisstudywastodeterminethecontributionofbioticandnon‐bioticfactorsto

cranberrypollination.Weperformedcomplementaryfieldandgreenhouseexperimentsto

comparetheeffectofbiotic(i.e.,beeorhandpollination)andnon‐bioticfactorssuchas

windormanualagitationonyield.Inthegreenhouse,wefoundthatplantsinthebiotic

treatmentproducedmoreberriesperupright,moreseedsperberry,andagreateroverall

yieldthanthenon‐biotictreatment.Plantsinthenon‐bioticagitationtreatment,however,

alsohadmoreberriesperuprightandoverallyieldthanplantsintheundisturbedcontrol

treatment.Inthefield,plantsinthebiotictreatmentproducedheavierberries,moreseeds

perberry,andagreateroverallyieldthanthenon‐bioticwindandagitationtreatments.

Plantsinthenon‐biotictreatmentsalsohadahigheryieldthantheundisturbedcontrol

treatment.Inboththegreenhouseandthefield,wefoundastrongcorrelationbetween

berryweightandnumberofseedsperberryfortheStevenscultivar.Theseresults

demonstratethatbothbioticandnon‐bioticfactorscontributesignificantlytocranberry

pollinationandthatcranberryisnotasdependentonpollinatorsaspreviouslybelieved.

Keywords(6):cranberry,Vacciniummacrocarpon,pollination,windpollination,thrips

1.0Introduction

Insectpollinationisanimportantecosystemservicerequiredbythemajorityof

floweringplants(Ollertonetal.2011).Beesarethemostimportantpollinators,butare

decliningworldwide(Biesmeijeretal.2006;NationalResearchCouncil2007;Pottsetal.

2010).InNorthAmerica,manyfarmersrelyonthemanaged,non‐nativehoneybee(Apis

mellifera)toprovidepollinationservices.Inthepast50years,however,managedhoney

beecolonieshavedeclinedover60%duetomites,disease,pesticideexposure,poor

nutrition,andstress(Ellisetal.2010).Nativebeesalsoprovideimportantpollination

servicesand,insomesystems,areabletoprovidesufficientpollinationwithoutthe

assistanceofhoneybees(e.g.,cranberry,Mohr&Kevan1987;watermelon,Winfreeetal.

2008).Unfortunately,nativebeesarealsoexperiencingdrasticdeclinesduetohabitat

destruction,intensifiedagriculture,agri‐chemicalexposure,anddisease(reviewedbyPotts

etal.2010).Withthedeclineofbees,farmersfacepossiblecropfailuresduetoinsufficient

pollination(Gallaietal.2009;Calderone2012).

Crops,however,varyinthedegreetowhichtheydependonpollinators,suggesting

thatnotallcropsareequallysusceptibletovariabilityintheabundanceofpollinators.

Whiletwothirdsofcropplantsrequireorbenefitfrominsectpollinationtoproduce

economicallyviablefruit(Kleinetal.2007),yieldresponsevariesbycrop.Intheabsence

ofpollinators,someplantsproducenofruit(e.g.,watermelon,Delaplane&Mayer2000),

whileothersproducemisshapen(e.g.,strawberries,Free1968;Jaycox1970)orsmallfruit

(e.g.,cherrytomato,Greenleaf&Kremen2006).Understandingthepollination

requirementsofspecificcropscanprovideinsightontheimpactofpollinatordeclineon

cropproduction.

Cranberry(Vacciniummacrocarpon)isconsideredtobeapollinatordependentcrop

(reviewedbyMcGregor1976;Eck1986,1990;Free1993;Delaplane&Mayer2000).

Althoughtheflowersareself‐compatible(Reader1977;Danaetal.1989;Sarracino&Vorsa

1991),pollenisreleasedbeforethestigmaisreceptive(Rigby&Dana1972),makingself‐

pollinationunlikely.Previousresearchshowsthatbeesareeffectivepollinatorsof

cranberry,capableofdepositingenoughpollenforfruitsetinoneortwovisits(Cane&

Schiffhauer2003).Asaresult,individualgrowersspendthousandsofdollarseachyearon

honeybeerentalstoensuresufficientpollination(USDANASSWASS2006).

Despitethewidespreaduseofhoneybeesandoveronehundredyearsofresearch,

thedegreetowhichcranberrydependsonpollinatorsremainsunclear.Althoughbeesare

efficientcranberrypollinatorsandcranberrydoesnotautogamouslyself‐pollinate(Cane&

Schiffhauer2003),itispossiblethatother,non‐bioticfactorscontributetocranberry

pollination.Fewstudies,however,haveconsiderednon‐beefactors.Ofthosethatdo,the

resultsareconflicting.Previousstudieshaveestimatedthataslittleas30%toasmuchas

100%ofthecranberrycropwouldbelostintheabsenceofbees(Robinsonetal.1989;

Southwick&Southwick1992;Williams1994;reviewedbyDelaplane&Mayer2000).At

oneendofthisrange,pollinatordeclineswouldhavelittleeffectoncranberryyield,while

attheotherendoftherange,therewouldbecropfailure.Furthermore,despiteclaimsthat

cranberrypollenistooheavytobetransferredbywind(Stricker1947),Papkeetal.(1980)

demonstratedthatthereisenoughcranberrypollenbeingcarriedinthewindandfalling

oncranberrymarshestopotentiallyprovideasignificantcontributiontopollination.And

Roberts&Struckmeyer(1942)demonstratedthatmanuallyagitatedcranberryplantsset

fruitintheabsenceofbees.Inlaterstudies,however,Filmer(1949)andMacKenzie(1994)

concludedthatwindorthemanualagitationofplantsdonotcontributetocranberry

pollination.Thepaucityofresearchinvestigatingnon‐beemechanismsofpollination,and

theinconsistencyinfindingsbetweenthestudiesthatdo,suggestthatwelackaclear

understandingofthefactorscontributingtocranberrypollination.

Thegoalofthisstudywastounderstandtherelativeimportanceofbioticandnon‐

bioticfactorstocranberrypollination.Wehypothesizedthatnon‐bioticfactorswould

resultinasufficientamountofpollentransfertoproduceaberrybutnotasmuchas

pollinationbybioticfactors.Toaddressthishypothesis,weestablishedfieldand

greenhouseexperimentsinwhichwemanipulatedbiotic(i.e.bees)andnon‐bioticfactors

(i.e.wind,manualagitation)thatmaycontributetocranberrypollination.Inthisstudywe

useyieldasametricofpollinationsuccesssincethisistheuniversalmetricusedin

agriculture.Weacknowledge,however,thatpollinationisonlyoneofmanyfactorsthat

mayaffectfinalyield.Bycomparingtheeffectofthesetreatmentsoncranberryyield,we

quantifiedtheindividualcontributionofeachfactortocranberryyield.

2.0Methods

2.1Cranberry

Cranberry(Vacciniummacrocarpon,Ericaceae)isaperennialfruitcropnativeto

NorthAmerica.Commerciallyitisgrowninartificiallycreatedmarsheswithsandy,acidic

soil.Cranberrygrowsinavininghabitalongthegroundandsendsupvegetativeand

floweringshoots(“uprights”).Eachfloweringuprightproducesupto8flowersthatbloom

sequentiallyfromthebottomoftheuprightupwardsoverseveralweeks(Eck1990).

Althoughcranberryflowerscontainbothmaleandfemaleparts,pollenisreleasedbefore

thestigmabecomesreceptive,makingautogamousself‐pollinationunlikely(Rigby&Dana

1972).Honeybeesarecommonlyusedforpollinationoncommercialcranberrymarshes

(Delaplane&Mayer2000).

2.2Greenhouse

Sixtydormantcranberryplantswithvisiblebuds,thirtyeachofthecultivars

“HyRed”and“Stevens”,weredugupfromacommercialcranberrymarshinlateMarchof

2012.Plantswererinsedthoroughlytoremoveallsandandpossiblepestsfromtheroots

andplantedinto15cmpotsofmoistpeatmoss.Potswerearrangedrandomlyina220C

greenhousewitha16hourphotoperiod.Approximatelyonemonthafterpotting,uprights

werethinnedsothatonlythosewith3‐5flowerbudsremained.Potswerefurtherthinned

to5‐6floweringuprightsperpotinordertoreducethetotalnumberofflowersinapot

andtoseparatethosethatremainedtomakehandpollinationpossible.Allbutthefirst

fourflowerstobloomperuprightweretrimmedoffastheyopenedsincecranberryplants

aremorelikelytosetfruitonthelower,earlierflowersthantheupperflowers(Birrenkott

&Stang1989).

Threetreatmentswereestablishedinthegreenhouse:(1)“hand”pollination,which

wasmeanttorepresentthebioticmovementofpollenbetweenflowers(mimickingbee

visitation),(2)“agitation”,whichwasmeanttorepresentthephysicalmovementofplants

bywind,and(3)anunmanipulatedcontrol,whichprovidedameasureofautogamousself‐

pollination.Toassessthepotentialforbioticpollination,flowerswithareceptivestigma

(i.e.thosethatweremoistandprotrudingfromthestamens)werehandpollinateddaily

duringbloombygentlyapplyingthestigmatoasmallaccumulationofpollencollected

fromyoungerflowersintothecapofamicro‐centrifugetube.Toassessthepotentialfor

non‐bioticpollination,plantsinthe“agitation”treatmentweregentlyjostleddailyduring

bloombymovingthepalmofthehandacrossthetopoftheuprights,causingtheplantsto

bumpagainsteachother.Thissimulatedthephysicalmovementofplantsasmaybe

causedbywindwhileexcludingthepossibilityofwindpollinationperseinwhichpollenis

movedthroughtheair.Plantsintheunmanipulatedcontroltreatmentwereleft

undisturbedthroughoutthestudytoassesswhetherfruitwouldbeproducedinthe

absenceofeitherbioticornon‐bioticfactors(i.e.,autogamousself‐pollination).Foreach

treatmentwehad10replicates(i.e.,pots)percultivar.Potswereplacedintwoparallel

rows~0.2mapartandspanning3‐3.5monbothsidesofasingleaisleofgreenhousetables

(onecultivarperside).Potsintherowclosesttotheaislewereassignedtothehand

pollinationtreatmentsothatallflowerswereeasilyaccessiblewithoutthepossibilityof

bumpingotherpots,andpotsinthebackrowwererandomlyassignedeithertothenon‐

bioticorundisturbedtreatment.Experimentaltreatmentswereinitiatedassoonasbloom

beganandwerecontinueddailyuntilallflowersweredoneblooming.Berrieswere

harvestedapproximatelytwomonthsafterbloombegan.Eachberrywasthenweighed

(wetweight,g)andthenumberofberriesperuprightwerecountedasaproxyforyield.In

ordertounderstandthelevelofpollinationreceivedineachtreatment,thenumberoffully

formedseedswascountedforeachberry.Cane&Schiffhauer(2003)demonstratedthat

thenumberofseedsisproportionaltotheamountofpollendepositedonthestigmaand

thereforerepresentsanindicationofpollinationsuccess.Averagesweretakenforeachpot

foratotalof10replicatespertreatment.

Toexaminedifferencesamongexperimentaltreatments(“hand”,“agitation”,

undisturbedcontrol)andcultivar(“Stevens”,“HyRed”),weusedafullyfactorialtwo‐way

analysisofvariance(ANOVA)tocompareberriesperupright,weightperberry,yield(total

berryweightperupright),andseedsperberry.Eachofthesevariablesindicatesomeform

ofpollinationsuccess.Differencesamongtreatmentsbycultivarweredeterminedusing

Tukey’sHonestlySignificantDifference(HSD)test(Hsu1996).Statisticalanalyseswere

performedwithJMPPro10.0.0(SASInstituteInc2007).

2.3Fieldcages

Toassesstheinfluenceofbioticandnon‐bioticfactorsoncranberryyieldinafield

setting,weestablishedacagestudyinacommercialcranberrymarshofthe“Stevens”

cultivar.Fourtreatmentswereestablished:(1)“open”,whichallowedbothbeevisitation

andagitationbywind,(2)“wind”,whichblockedinsectvisitationwithafinenylonmesh

(mattenylontulleinivory,JoannFabric)butallowedwindtoagitatetheplantsormove

pollen,(3)“closed”,whichpreventedinsectvisitationandwindusingfloatingrowcover

(Agribon+AG‐15InsectBarrier,Johnny’sSelectedSeeds)withacorrugatedplasticwind

blocksurroundingthecage(4mmcorrugatedplastic,LairdPlastics),and(4)“agitation”,

whichusedthesamecagedesignasthe“closed”treatmentbutreceivedmanualagitation

twiceperweekduringbloomtomimicmovementoftheplantsbywindbutexcludedthe

possibilityofwindpollinationperseinwhichpollenismovedthroughtheair.Each

treatmentwasreplicated10times.Cageframeswereconstructedusinglightweight,black

irrigationtubingand¾”PVCcutinto6”segmentswithapointatoneend(i.e.12”PVC

sectionswerecutinhalfata45oangle).ThePVCstakeswerehammeredintothegroundat

eachcornerofeachcageandtheirrigationtubingwasinsertedintothePVCtomakeatent

shapeframe.Meshwasattachedtothecageframesusing2”binderclips.Asmallsheetof

2mmplasticsheetingwasplacedbetweenthebinderclipandthemeshtopreventthe

meshfromtearing.Themeshwasfurthersecuredbyplacing½”‐¾”PCVsegmentsfilled

withgravelandsandatthebaseofeachsideofthecage.Inordertoaccountforpossible

differencesinplantsasafunctionoflocationwithinthecranberrybed,cageswere

arrangedinagridandtreatmentswereassignedusingamodifiedLatinSquaredesignwith

eachtreatmentoccurringoncepercolumnandtwiceperrow.Cagesweresetupbefore

cranberrybloom(May25,2012)andremovedwhenbloomwascomplete(July9,2012).

Berrieswereharvestedfroma0.3mx0.3m(1ft2)plotfromthecenterofeachcagebefore

harvest(September20,2012)andcountedandweighed(wet)toestimateyield.Wet

weightwasusedasthiscanbeeasilyconvertedtoyieldunitsusedbycranberrygrowers

(barrels/acre,1barrel=100lbs=45kg).Twentyberriesfromeachcagewerealsocutin

halfwitharazorbladeandallfullyformedseedswithinwerecounted.

Anadditional15cages(5each“open”,“wind”,and“closed”,treatmentsasdescribed

above)wereestablishedtomeasureenvironmentalvariablesthatmaybealteredbythe

cagesincludingtemperature,lightintensity,soilmoisture,andinsectcommunity.

Temperatureandlightintensityweremeasuredevery30minutesforthedurationofthe

cagestudyusingHOBOdataloggers(OnsetComputerCorporation)hunginsideStyrofoam

sunshields.SoilmoisturewasmeasuredusingaTDR300soilmoisturemeter(Spectrum

Technologies,Aurora,Illinois)twiceduringthegrowingseason(June14andJuly9,2012).

Fourmeasurementsweretakenpercage.Theinsectcommunitywasmeasured

continuouslyduringbloomusingyellowstickystrips(3”x5”,GreatLakesIPM025‐SS‐35)

andblue,yellow,andwhitepantraps(ACEBrandFluorescentpaint)containingsoapy

water(Dawnbluedishsoap).

Toexaminedifferencesamongtreatmentsforberriesperupright,weightperberry,

yield,andseedsperberry,weusedaone‐waymixedmodelANOVAwithrowandcolumn

locationsasrandomeffects.DifferencesamongtreatmentsweredeterminedusingTukey’s

HSDtest.StatisticalanalyseswereperformedusingJMPPro10.0.0(SASInstituteInc.

2007).

3.0Results

3.1Greenhouse

Inthegreenhouse,significantfruitsetoccurredonplantsinboththebiotic(“hand”)

andnon‐biotic(“agitation”)treatmentsbutnottheundisturbedcontrol.Ninety‐eight

percentof“HyRed”and92%of“Stevens”uprightsinthe“hand”pollinationtreatment

producedfruitand52%ofthe“HyRed”and30%ofthe“Stevens”uprightsinthe“agitation”

treatmentproducedfruit.Only2%of“HyRed”and5%of“Stevens”uprightsinthe

unmanipulatedcontrolproducedfruit,providingevidenceforthelackofautogamousself‐

pollinationincranberry.

Thenumberofberriesperuprightvariedsignificantlyamongtreatmentsinboth

cultivars(treatment,F2,58=248.6,p<0.0001,Fig.1a).Significantlymoreberriesperupright

wereproducedinthe“hand”pollinationtreatmentthaninthe“agitation”treatment,and

moreininthe“agitation”treatmentthanintheunmanipulatedcontrol.Thisdifference

wasgreaterinthe“HyRed”cultivarthanin“Stevens”(treatmentxcultivar,F2,58=3.9,

p=0.028).Berryweightdidnotvaryacrosstreatments(F2,41=2.4,p=0.11,Fig.1b)or

cultivar(F1,41=0.0021,p=0.96).Thenumberofseedsperberrywasgreaterinthe“hand”

pollinationtreatmentthanbothoftheothertreatmentsanddidnotvarybetweenthe

“agitation”treatmentandtheunmanipulatedcontrol(F2,58=136.3,p<0.0001,Fig.1c).The

numberofseedsperberryfortheundisturbedtreatmentin“HyRed”isbasedonasingle

berrythatformedinthistreatmentandisthereforenotrepresentativeofthetreatmentas

awhole.Yieldwasestimatedbytotalberryweightperuprightwhichisafunctionofberry

weightandberriesperupright.Overall,yieldswerehigherinthe“hand”pollination

treatmentthanintheothertreatments(treatment,F2,58=210.3,p<0.0001,Fig.1d).Total

berryweightperuprightwasalsosignificantlygreaterinthe“agitation”treatmentthanthe

“no‐pollination”treatmentfor“HyRed”butnotfor“Stevens”.

3.2Fieldexperiment

Inthefield,openplotshadthehighestfruitset,althoughevenwheninsectswere

excluded,therewassubstantialfruitsetinbothofthenon‐biotictreatments(“agitation”

and“wind”).Thenumberofberriesperuprightwasfairlyconsistentacrosstreatments

anddidnotvarybetweenthe“open”treatmentandanyothertreatmentbutwaslowerin

the“agitation”treatmentthaninthe“wind”or“closed”treatments(treatment,F3,24.6=4.6,

p=0.011,Fig.2a).Theweightperberrywassignificantlydifferentamongtreatments(F‐

3,24.2=36.6,p<0.0001,fig.2b)withtheheaviestberriesinthe“open”treatment,followedby

“agitation”,andlowestinthe“wind”treatmentand“closed”control.Thenumberofviable

seedsperberryvariedsignificantlybytreatment(F3,23.91=64.9,p<0.0001,Fig.2c)withthe

mostfoundinthe“open”treatmentfollowedby“agitation”andtheleastin“wind”and

“closed”treatment.Yield,asestimatedfromsmallplots,washighestforthe“open”

treatmentfollowedby“wind”and“agitation”andlowestforthe“closed”treatment

(F3,23.1=70.5,p<0.0001,fig.2d).

Becausethenumberofseedsisproportionaltotheamountofpollendeposited

(Cane&Schiffhauer2003),weusedseedsperberryasameasureofpollinationsuccess.

Wefoundastrongrelationshipbetweenberryweightandseednumberfor“Stevens”in

boththegreenhouse(p=0.0011,R2=0.42,fig.3a)andthefield(R2=0.83,p<0.0001,fig.3a)

butnotfor“HyRed”(p=0.39,R2=0.04,fig.3b).Thispatternsuggeststhatthenumberof

pollentetradsdepositedonflowersvariedsignificantlyamongtreatmentsandthatevenin

the“open”treatment,pollencanbelimited,preventingtheberryfromreachinga

maximumweight.

3.2.1Environmentaleffects

Theenvironmentalvariableswemeasuredtotestcageeffectsprovideevidencethat

thecagessuccessfullyexcludedpollinatorswhilemaintainingcomparableconditions

withineachcagetype.Theabundanceofinsectsvariedsignificantlyamongalltreatments

withthelowestabundanceinthe“closed”(rowcover)treatment,suggestingthatcage

treatmentseffectivelyexcludedallbutthesmallestinsects(e.g.,thrips).Soilmoisturedid

notvaryamongcagetreatments(F2,23=0.17,p=0.84).Thetemperaturewasonaverage

1.1oChigherinthe“closed”treatmentcagethantheopenor“wind”(nylonmesh)

treatments(F2,7038=13.5,p<0.0001).Lightvariedsignificantlyaswellwiththemostlightin

theopentreatmentfollowedequallybythe“wind”and“closed”treatments(F2,13163=42.4,

p<0.0001).Shadingcanresultinahigherproductionofvegetativematerialresultingin

loweredyields(RobertsandStruckmeyer1942).

4.0Discussion

Therequirementofbeesforcranberrypollinationisgenerallyassumedalthough

theevidenceislacking.Inoveronehundredyearsofresearch,onlyfourstudieshave

consideredthecontributionofnon‐beefactorstocranberrypollination(Roberts&

Struckmeyer1942;Filmer1949;Papkeetal.1980;MacKenzie1994).Inthisstudywe

demonstratethatintheabsenceofbees,cranberryisstillabletoproducefruit.Inafield

setting,wefoundthatplants,fromwhichinsectpollinators,butnotwind,wereexcluded,

producedagreateroverallyieldthanplantsfromwhichbothinsectsandwindwere

excluded.Thisfinding,combinedwithmanualagitationtreatmentsinthefieldand

greenhouse,challengesthenotionthatbeesaretheonlywayforcranberrytoproducefruit

(reviewedbyMcGregor1976;Eck1990;Free1993;DelaplaneandMayer2000),and

suggeststhatbothbioticandnon‐bioticfactorscontributesignificantlytocranberry

pollination.

Previousresearchoncranberrypollinationhasmainlycomparedtheeffectofbee

pollinationversusautogamousself‐pollination.Themajorityofthesestudieshave

concludedthatbeesarerequiredtoproducefruit,althoughwhattheirdataactually

demonstrateisthatcranberriesarenotautogamousandareunabletoself‐pollinatewithin

asingleflower(Hutson1925;Farrar&Bain1947;Filmer&Doehlert1959;Marucci1966;

Marucci&Moulter1977;Cane&Schiffhauer2003).Ourstudysupportsthefindingthat

cranberrydoesnotautogamouslyself‐pollinate,butalsoprovidesevidencethatother,non‐

beefactorsplayaroleincranberrypollination.

Theincreasedyieldinthenon‐biotictreatments(i.e.agitation,wind)ascompared

totheclosedtreatmentinthefieldmaybeattributabletouncontrolledvariablesinthefield

suchasnon‐beeinsectpollinators,agronomicvariation(i.e.uprightdensity),ora

combinationofthetwo.Inthegreenhouse,theagitationtreatmentproduced

approximately25%oftheyieldcomparedtothehandpollinationtreatment,whereasthe

no‐pollinationtreatmenthadvirtuallyzeroyield.Inthefield,thenon‐biotictreatments

producedapproximately50%oftheyieldcomparedtotheopentreatment,andeventhe

no‐pollinationtreatmenthadsomeyield.Throughcarefulcageconstructionandpan

trappingwithincages,weareconfidentthatbeeswerenotcontributingtotheincreased

yieldwithinthefieldcagetreatments.However,thrips,tinypollen‐eatinginsects,were

foundinalltreatmentsinthefieldandhavebeenshowntobeeffectivepollinatorsinother

systems,includingEricaceousplantswhichareinthesamefamilyascranberry(Hagerup&

Hagerup1953;Kirk1988;Baker&Cruden1991;Ananthakrishnan1993),althoughtheir

influenceincranberrypollinationhasnotbeeninvestigated(butseeAppendix1.1).The

absenceofthripsinthegreenhouse(pers.obs.)andabundanceinthefieldsuggeststhat

theymaybeacontributingfactor.

Anotherfactorthatmayhavecausedincreasedyieldinthenon‐bioticandclosed

treatmentsinthefieldisfloweringuprightdensity.Inthegreenhouse,floweringuprights

werethinnedtoaverylowdensitytomakehandpollinationmanageable(279flowering

uprights/m2),whereasinthefield,floweringuprightsweresixtimesasdense(1705

floweringuprights/m2).Withahigherdensityoffloweringuprights,pollenismore

abundantandflowersareclosertogether,increasingthelikelihoodthatpollencouldbe

transferredbetweenflowerswithevenslightagitation.Ahighdensityofuprightsnotonly

increasestheprobabilityofpollentransferbetweenflowerswhenagitated,butmayalso

makemovementofthripsamongflowerseasier.

Anotherdifferencebetweenthefieldandgreenhousewasthepatternamong

treatmentsinberryweight.Inthefield,berryweightwassignificantlydifferentamong

treatments,whereasinthegreenhouse,berryweightdidnotvaryamongtreatments.

Previousstudieshavefoundastrongcorrelationbetweenberryweightandseednumber

(Hall&Aalders1965;Rigby&Dana1971),demonstratingthatwhenpollenislimited,

berryweightislow.Inourstudy,wefoundasignificantrelationshipbetweenberryweight

andseednumberintheStevenscultivarinthefieldandthegreenhouse,althoughthe

relationshipwasweakerandshallowerinthegreenhouse.Despiteevidenceinprevious

studiesthatcranberrycanproduceseedlessfruitthroughparthenogenesis(Roberts&

Struckmeyer1942),evenberriesintheno‐pollinationtreatmenthadsomeviableseeds,

suggestingthatparthenogenesisisnotoccurringhere.Additionally,thenumberofseeds

perberrywassimilarbetweentreatmentsinthefieldandgreenhouse,suggestingthat

otherfactors,suchaswaterandnutrientavailabilityandnotjustpollenlimitation,may

playaroleinberryweight.Thelackofrelationshipbetweenberryweightandseed

numberintheHyRedcultivarinthegreenhousefurthersuggeststhatberryweightis

influencedbyfactorsotherthanseednumber.CaneandSchiffhauer(2003)foundthatin

theStevenscultivar,theberryreachesamaximumweightwhentheflowerreceives8

tetradsofpollenresultinginabout15seeds.Inourstudy,berriesintheStevenscultivar

onlyreached15seedsperberryinthehandpollinatedtreatmentinthegreenhouse,

suggestingthatevenintheopentreatmentinthefield,pollenmaybelimited.InHyRed,

however,therelationshipwasflatsuggestingthattheseednumber/berryweight

relationshipmayvaryamongcultivars.

Previousstudies,onwhichcurrentpollinationmanagementrecommendationsare

derived(McGregor1976),weredesignedtotesttheimportanceofbeestocranberry

pollinationbutdidnotaccountforthepossibilityofnon‐beepollinationvectors.Other,

morerecentstudies(e.g.,CaneandSchiffhauer2003)havedemonstratedtheefficiencyof

beepollinatorsandthelackofautogamousself‐pollinationincranberry,butstilloverlook

alternativemechanismsforpollination.Phillips(2011)alsodemonstratedthelackof

autogamousself‐pollinationincranberrybutincorrectlyconcludedthatcranberryrequires

insectpollination.Inthesestudies,individualcranberryflowerswereisolatedto

demonstratetheinabilitytoself‐pollinate.However,inthefield,flowersarenotisolated,

rathertheyareexposedtoavarietyofbioticandnon‐bioticfactors.Inseveralinfluential

studies,Hutson(1925)andFilmerandDoehlert(1955)demonstratedthedependenceof

cranberryonbeesinafieldcagestudy,butwhenberriesformedwithinthecages,

attributedtheberriestofaultycagesratherthanconsideringalternativemechanismsof

pollination.

Ourstudywasspecificallydesignedtotesttheco‐existenceofpollination

mechanismsincludingbees,wind,mechanicalaction,andautogamousself‐pollination.We

foundthatmechanicalagitationbywindorhand,caneffectivelymovepollenbetween

cranberryflowers.Insmallplotsatourstudysite,asmuchas50%ofyieldcouldbe

attributedtonon‐beepollinators,resultingineconomicallycompetitiveyields.Theresults

ofthisstudysuggestthatintheabsenceofbeepollinators,cranberrygrowersmaystillbe

abletoproduceasignificantcropyield.Theseresultsfurthersuggestthatmechanical

agitationmaybemoreprevalentinothercroppingsystemsthanpreviouslybelievedand

providesfurtherrationalefordetailedpollinationstudiesinothercropplants.

Acknowledgements

TheauthorswouldliketothankC.J.SearlesCranberryInc.forallowingustoconductour

fieldcagestudyontheirmarshandGaynorCranberryforprovidingplantmaterialforthe

greenhousestudy.WethankEricZeldinforhisassistancediggingplantmaterialand

providingguidanceonestablishingtheplantsinthegreenhouse.Wealsothankthefield

andlabassistantswhoassistedwiththisproject:RachelMallinger,AmandaRudie,Collin

Schwantes,EricWiesman,ChristopherWatson,SachaHorn,andScottLee.Fundingforthis

researchwasprovidedbyaHatchGranttoC.G.

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Figurecaptions

Figure1:Metricsofpollinationsuccessforthecranberrycultivar“HyRed”and“Stevens”as

measuredinthegreenhouse:(a)thenumberofberriesperupright(mean±SE),(b)the

berryweight(mean±SE),(c)thenumberofseedsperberry(mean±SE),and(d)theyield

estimate(meanwetweightperupright±SE).Treatmentsincluded“hand”pollination

whichrepresentedbioticpollination,“agitation”whichrepresentednon‐bioticpollination,

andanundisturbedcontrol.

Figure2:Metricsofpollinationsuccessforthecranberrycultivar“Stevens”asmeasuredin

thefield:(a)thenumberofberriesperupright(mean±SE),(b)theberryweight(mean

±SE),(c)thenumberofseedsperberry(mean±SE),and(d)theyieldestimate(mean±SE).

Treatmentsincluded“open”pollinationwhichrepresentedambientpollination,“wind”

whichrepresentednon‐bioticpollinationthroughwindpollinationperseandphysical

movementoftheplantsduetowind,“agitation”whichrepresentednon‐bioticpollination

duetophysicalmovementoftheplantsintheabsenceofwindpollinationperse,anda

closedcontrol.

Figure3:Relationshipbetweenberryweightandseedsperberryforthecranberry

cultivars(a)“Stevens”and(b)“HyRed”.

Figure 1

agitationhandpollination

undisturbed

HyRed cultivarStevens cultivar

undisturbedW

Cagitationhand

pollinationundisturbed

undisturbed

Cage Treatment

agitationwindopen closed

Figure 2

Cage Treatment

agitationwindopen closed

agitationwindopen closed agitationwindopen closed

150100500

300250

(a) Stevens cranberry cultivar

(b) HyRed cranberry cultivar

Figure 3

Greenhouse

Seeds/berry

200 5 10 15

Field Greenhouse

openagitation

closedwind

openagitationundisturbed

Appendix1.1:Assessingtheroleofthrips(Thysanoptera)incranberrypollination

Introduction

Cranberryisconsideredapollinatordependentcrop(DelaplaneandMayer2000),

butinfieldexperimentsin2011and2012,caged(“closed”)cranberryplantsproduceda

significantamountoffruit.Inafollow‐upgreenhousestudy,plantsinthe“closed”

treatmentproducednearlynofruitatall.Theseresultssuggestthatadditional,

uncontrolledfactorsexistinthefieldthateffectcranberrypollination.Onepossiblefactor

isthepresenceofthrips,tinypollen‐eatinginsects.Thripsareknowntobeimportant

pollinatorsinsomesystems(Kirk,W.D.J.1988,BakerandCruden1991,Ananthakrishnan

1993)andwerefoundonstickycardsinallfieldtreatmenttypes(Gaines,unpubl.data).

Anotherfactorthatmayinfluencepollinationisthedensityoffloweringuprights.Field

plotshadasignificantlyhigherdensityoffloweringuprightsascomparedtothe

greenhouse.Ahigherfloweringuprightdensitycouldmakemovementofthripsfromone

planttoanothereasierorsimplyincreasetheprobabilitythatflowersbumpintoeach

otherwhenagitated.Therefore,theobjectiveofthisstudywastodeterminethe

contributionofthripsandtheinfluenceofuprightdensityoncranberrypollination.

Methods

Cranberries

CranberryplantsofthecultivarStevensweredugfromacommercialcranberry

marshinlatefall2012.Sincethegroundinthemarshwasalreadyfrozen,plantswereonly

Table1:Numberofpotspertreatmentforintendedstudydesign

collectedattheedgeofthemarshwherechunksofplantscouldbeextractedwithanice

pick.Plantswerebroughtbacktothegreenhouseandkeptincoldstorage(4oCwithan8‐

hourphotoperiod)foronemonth.Icewasplacedovertheplantsonceperweektokeep

theplantsfromdryingout.

Afteronemonthincoldstorage,theplantswererinsedoffandtransplantedinto6”

potsfilledwithmoistpeat.Potsweresetina220Cgreenhousewitha16hourphotoperiod

andassignedatreatment(table1).Plantswerewateredevery4daysandexcessivevine

growthtrimmed.Afteraboutthreeweeks,plantswerefertilizedwith½teaspoon

fertilizerpergallonwater.

Thestudywasintendedtobea2‐

factor,fullfactorialdesigntocomparefruit

setduetohandpollination,thrips

pollination,agitation,andnopollinationas

afunctionofuprightdensity.Tenpots

wereassignedtoeachtreatment(table1).

Approximatelyfourweeksafter

potting,plantswereexpectedtobeginshowingsignsofflowerdevelopment.

Unfortunately,veryfewplantsdidsoandtheexperimentaldesignhadtobedrastically

reduced(table2).Thiswaslikelyduetopoorplantmaterialdugfromthemarshinthefall.

Becauseofthefrozenground,wewereunabletobeselectiveinwhichplantswedug.The

plantsthatdidshowsignsoffloweringwereplacedintolargecageswithfinemeshtokeep

Uprightdensity

Low High

Pollination

treatment

Hand 10 10

Thrips 10 10

Agitation 10 10

None 10 10

Table2:Numberofpotspertreatmentforactualstudydesign.

thripsinorout.Eachcagehadtwopotswithsixcagespertreatment(n=12potsper

treatment).

Thrips

Oncethecranberryplantswerere‐

pottedintopeat,athripscolonywas

establishedinthelab.Tostartthecolony,a

fewdozengreenbeanscontainingthrips

eggswereacquiredfromanexistingcolony.

Thecolonywasmaintainedusing

previouslyestablishedmethods(Tom

German,pers.comm.)asfollows.Twotothreeofthebeansfromtheestablishedcolony

wereplacedinplasticdelicupswithmeshtops.Freshbeanswerepurchasedandsoaked

for10minutesinableachsolution(50mLbleachto500mLwater)tokillany

microorganismsandpreventmoldingonthebeans.Oncedry,twotothreefreshbeans

wereaddedtoeachdelicuptoprovidefoodforemergingthrips.Freshbeanswereadded

andoldbeansremovedevery~4days.

Whencranberrybloombegan,plantsinthe“thrips”treatmentwereinoculatedwith

3lateinstaroradultthripsperflower.Thripsweretransportedtothegreenhouseusing

centrifugetubes.Tubeswerestuckintothesoilofthepotsinthethripstreatmentandthe

capsremovedtoallowthethripstocrawlontothecranberryplants.Thiswasdonetwice

duringthethreeweekbloom.Plantsinthenopollinationtreatmentwereleftundisturbed.

Uprightdensity

Low High

Pollination

treatment

Hand 0 0

Thrips 0 12

Agitation 0 0

None 0 12

Afterbloom,bluestickycardswereplacedineachcagetoverifythepresenceof

thrips(Chenetal.2009).Wealsointendedtocountandmeasureberriesoncetheywere

fullsize.Thisneverhappenedbecausenoberriesformedonanyplantsineithertreatment.

Results

Nocranberryfruitswereproducedineithertreatment(table3).Wewerealso

unabletorecaptureanythripsonthebluestickycardsineitherthecagesorintheopen

greenhouse.

Pots Berriesperupright

Thripsperstickycard

Pollination

treatment Thrips 12 0±0 0±0

None 12 0±0 0±0

Conclusions

Theresultsofthisstudyareunabletosupportthehypothesisthatthripscontribute

tocranberrypollination.Itispossiblethatthripsarenotcontributingtocranberry

pollinationorthatexperimentaldesignfailedtoeffectivelytestthis.Futurestudiesshould

digcranberryplantsearlierinthefallorinthespringtoallowforbetterplantmaterial

selection(i.e.,plantswithlargebudspresent).Additionally,insteadofinoculatingplants

withthrips,placingplantsingreenhouseswithknownthripsinfestationsmaybemore

Table3:Resultsfrompollinationstudy

effective.Thripsareaseriousgreenhousepestandfindingagreenhousewiththrips

problemshouldnotbedifficult.

Literaturecited

Ananthakrishnan,T.N.1993.Theroleofthripsinpollination.CurrentScience65:262–264.Baker,J.D.,andR.W.Cruden.1991.Thrips‐MediatedSelf‐PollinationofTwoFacultatively

XenogamousWetlandSpecies.AmericanJournalofBotany78:959–963.Chen,T.‐Y.,C.‐C.Chu,G.Fitzgerald,E.T.Natwick,andT.J.Henneberry.2009.Trap

EvaluationsforThrips(Thysanoptera:Thripidae)andHoverflies(Diptera:Syrphidae).EnvironmentalEntomology:1416–1420.

Delaplane,K.S.,andD.F.Mayer.2000.Croppollinationbybees.CABIPublishing,New

York,NY.Kirk,W.D.J.1988.Thripsandpollinationbiology.inAnanthakrishnan,T.N.andRaman,A.,

editors.DynamicsofInsect‐PlantInteraction:RecentAdvancesandFutureTrends.Oxford&IBHPublishingCompany,NewDelhi.

CHAPTER2

Thecontributionofhoneybeestocranberryyieldvarieswiththeamountof

woodlandinthesurroundinglandscape

Author:HannahR.Gaines

Co‐author(s):PaulD.MitchellandClaudioGratton

Forsubmissionto:JournalofEconomicEntomology(“apicultureandsocialinsects”or

“horticulturalentomology”section),EcologicalApplications,FrontiersinEcology,or

Ecosphere

Abstract:Two‐thirdsofcropplantsrequireorbenefitfrominsectpollination.Toensure

sufficientpollinationoftheircrops,manyfarmersrenthivesofhoneybees.Cranberry

(Vacciniummacrocarpon),aperennialfruitcropnativetoNorthAmerica,isgenerally

consideredpollinatordependentandmostcranberrygrowersrenthoneybeesfor

pollination.Theeconomicallyoptimalhivestockingdensity,orthepointatwhichthecost

ofaddinganadditionalhiveisgreaterthantheeconomicreturn,however,isunknown,

resultinginwidevariationinmanagementpractices.Therecommendedstockingdensity

is4.9‐7.4hives/ha(2‐3hives/ac),butsomeWisconsincranberrygrowersrentasmanyas

22hives/ha(9hives/ac).Anotherexplanationforthisvariationinmanagementisthatthe

economicallyoptimalstockingdensityvariesdependingonthesurroundinglandscapedue

todifferinglevelsofbackgroundpollinationbynativebees.Therefore,theobjectiveofthis

studywastodeterminetherelationshipbetweencranberryyieldandhoneybeehive

stockingdensityandwhetherthisrelationshipisconsistentacrossthelandscape.To

addressthisobjective,wecollectedhistoricalproductionrecordsfromWisconsin

cranberrygrowersregardingtheuseofhoneybeesandcranberryyieldfor2000‐2011.We

foundastrongpositiverelationshipbetweenyieldandhives/habutonlywhenthe

proportionofwoodlandwithin1kmofthecranberrymarshwaslow(<41.6%).

Furthermore,thevariationinyieldatmarshesinlow‐woodlandlandscapesdecreasedas

thenumberofhivesincreased,indicatingthatincreasinghivesleadstohigheryieldswith

lessvariationinthatyield.Althoughtherewasnoevidencethatincreasinghiveswas

beneficialatmarshesinhigh‐woodlandlandscapes,theyieldatthesemarsheswhenhoney

beeswereabsentwasmarginallyhigherthanatmarshesinlow‐woodlandlandscapes.

Overtherangeofhivesobserved,wewereunabletodeterminetheoptimalhivestocking

densityalthoughWisconsincranberrygrowerswithmarshesinlow‐woodlandlandscapes

canexpectincreasingreturnsonyielduptoandabove17hives/ha(7.6hives/ac).The

valueofeachadditionalhivewas1098kg/hive(24.2bbl/ac)atmarshesinlow‐woodland

landscapesand0kg/hiveinhigh‐woodlandlandscapes.Theseresultssuggestthatthe

habitatsurroundingacranberrymarshinfluencestheeffectivenessandeconomically

optimalstockingdensityofhoneybeesforcranberrypollination.

Keywords:honeybees,Apismellifera,cranberry,hivestockingdensity,pollinator

1.0 Introduction

Pollinationisanimportantecosystemservicevaluedat$15billion/yeartoUS

agriculturealone(Calderone2012).Two‐thirdsofcropplantsrequireorbenefitfrom

insectpollination(Kleinetal.2007)andprovidethemainsourceofseveralkeyvitamins

andmineralsinthehumandiet(Eilersetal.2011).Asaresult,managedhoneybeesare

widelyusedinmanyagriculturalsystemsforcroppollination.Honeybees(Apismellifera)

occurinlargecolonies,areeasytomanage,andwillvisitmanydifferentplantspecies,

makingthemanidealspeciesforpollinationinmodernagriculturalsystems(Kremenand

Chaplin‐Kramer2007,Calderone2012).Nativebeesarealsoeffectivecroppollinators,but

occurinsmallnumbers,aremoredifficulttomanage,andoftentimesarespecialized

pollinatorsofoneplantfamilyorgenus(DelaplaneandMayer2000,Michener2000).Even

so,nativebeesaloneareabletoprovidefullpollinationservicesinsomesystems(e.g.,

watermelon,Winfreeetal.2008,cranberry,MohrandKevan1987).

Cranberryisonecropwherehoneybeesarecommonlyusedtofulfillpollination

requirements,althoughhivestockingdensitiesvarygreatly.Currentmanagement

recommendationsforWisconsincranberrycallfor4.9‐7.4hives/ha(2‐3hives/ac,

McGregor1976),butgrowersuseanywherefrom0‐22hives/ha(0‐9hives/ac,H.Gaines,

pers.obs.).Oneexplanationforthevariationinmanagementpracticesmaybethatsome

marsheshaveahigherlevelofbackgroundpollinationratesduetothepresenceofnative

beesandthereforedonotrequireasmanyhoneybees.Previousstudieshavealsoshown

thatsomenativebeesare,infact,moreefficientcranberrypollinatorsthanhoneybees

(CaneandSchiffhauer2003).Additionally,currentmanagementrecommendationsare

basedonresearchfromover50yearsagowhenyieldsweremuchlower,landscapeswere

lessdeveloped,andthepollinationrequirementsofcranberrywerenotfullyunderstood,

resultinginconflictingrecommendations.Forexample,FilmerandDoehlert.(1955)

suggestusing0.5hives/ha(1hive/5ac)whereasFarrarandBain(1947)suggestfrom2.5‐

24.7hives/ha(1‐10hives/ac).Changesintechnologyandmanagementpracticesalong

withabetterunderstandingofthepollinationrequirements(Gaineschp.1)suggestthat

updatedrecommendationsmaybeneeded.Furthermore,economictheoryregarding

optimalinputuseimpliesthattheoptimalstockingdensitywilldependonthecropprice

andthecostofrentinghives(Beattieetal.2009).Theoptimalinputisreachedwhenthe

costofaddinganadditionalhiveexceedstheeconomicreturnofaddingthathive.

Onefactorthatmayinfluencetheoptimalstockingdensityforhoneybeesisthe

amountofnaturalhabitatinthesurroundinglandscape.Previousstudieshaveshownthat

nativebeesrespondpositivelytoamountofandproximitytonaturalhabitatandthat

pollinationservicesandyieldincreasewithbeediversity(Kremenetal.2002,Rickettsetal.

2008).Therefore,cranberrymarsheswithmorenaturalhabitatinthesurrounding

landscapemayhavehigherbackgroundpollinationratesthanmarsheswithlittlenatural

habitat,reducingtheamountofhoneybeesrequired.Thehypothesisthatoptimalhive

stockingdensitiesvarywithlocalconditionsissupportedbythelargevariationin

managementpracticesobservedinWisconsinandthefactthataveragestockingdensities

forcranberryalsovarybygrowingregion(R.Serres,pers.comm.).

Cranberrygrowersspendasignificantamountofmoneyonpollinationservices,but

sincetheoptimalhivestockingdensityisunknown,theymaynotbespendingtheirmoney

inanefficientway.Becauseofthemagnitudeofthecostofhoneybeehiverentals,

determiningtheoptimalhivestockingdensitywouldallowgrowerstomaximizetherateof

returnontheirinvestmentinhivesandpotentiallysavethemthousandsofdollarsevery

year.Thegoalofthisstudywastodeterminetheeconomicallyoptimalhoneybeehive

stockingdensityforWisconsincranberryandwhetherthisrateisconsistentacrossthe

landscape.WeusedhistoricaldatafromWisconsincranberrygrowerstodetermine(1)the

relationshipbetweencranberryyieldandhoneybeehivestockingdensity,(2)themarginal

valueofeachadditionalhiveofhoneybeesforcranberryyield,and(3)iftheeconomically

optimalrateremainsconstantacrossthelandscape.

Methods

2.1Growerdata

Datawerecollectedfrom38cranberrygrowers,eitherthroughpreviously

establishedgrower‐collaboratorsorothergrowersreachedthrougharequestattheannual

meetingoftheWisconsinStateCranberryGrowersAssociation(WSCGA).Growerswere

askedtocompleteaworksheetincludinginformationonmarshlocation,establishment

year,varietiesgrown,areaincranberryproduction,honeyandbumblebeeuse,andyield

recordsfortheperiod2000‐2011.Becausecranberrytakesabout3yearsfrommarsh

establishmenttoproduceacrop,onlydatafrommarshesmorethan3yearsoldwereused.

Datafromyearsinwhichsignificantdamagetothecropduetopestsorhailwasrecorded

wereexcluded.Datafromyearsinwhichgrowerswerefollowingamarketingorder

volumecontroltoreduceyieldwerealsoexcluded.Amarketingordervolumecontrolisa

toolusedbyagriculturalindustriestoreducetheover‐productionofacropbylimitingthe

amountofcropagrowercansell(JesseandRogers2006).Thisresultedinadatasetwith

38uniquegrowerswithanaverageof9.6years(min.1‐max.12years)ofyieldandhive

data.Thedatathatwerereportedincludedtotalacresofcranberrycultivated,total

numberofhivesrented,andtotalcranberryharvestinbarrels(1bbl=100lbsor45.4kg)

foreachyear.Ithenconvertedthesedatatohives/haandyield/ha.

2.2Landscapedata

Sinceotherdatasetssuggestthatwoodlandisagoodpredictorvariablefornative

beesandtheirpollinationservices(Gaineschp.3),Icalculatedtheproportionwooded

habitatwithin1kmofeachmarshusingtheCroplandDataLayer(USDA2011)andArcGIS

10.0(ESRI2011).Acentroidwaslocatedinthecenterofeachmarshanda1kmradius

drawnaroundthatpoint.Nativebeeabundanceandspeciesrichnessispositively

associatedwithnaturalhabitatinthesurroundinglandscape(Gaineschp.3),sowooded

habitatwasusedasaproxyforbackgroundnativepollinatorspresentinthelandscape.

2.3Statisticalanalyses

Todeterminetherelationshipbetweencranberryyield(kg/ha)andhoneybeehive

stockingdensity(hives/ha)asafunctionofthepercentwoodlandwithina1kmradius

aroundeachmarsh,weusedamultiplemixedmodellinearregressionwithhives/ha,

percentwoodland,andtheirinteractionasfixedeffectsandfarmasarandomeffect.Since

theinteractiontermbetweenhives/haandwoodlandcategorywassignificant(p=

0.0003),theanalysiswasalsoconductedseparatelyusingthedatafrommarshesinhigh‐

andlow‐woodlandlandscapes.AShapiro‐WilkGoodnessofFittestonyieldindicatedthat

thedatawerenormallydistributed(W=0.993,p=0.0757),sonotransformationswere

used.Atermforyearandsecondordertermforhives(anindicationofcurvature)were

initiallyincludedinthemodelbutwerefoundnotsignificantandwerethereforedropped

fromthefinalmodel(year,p=0.095F1,212.1=2.82,hives2,p=0.50F1,205.1=0.45).

Todeterminewhetherthevariationinyieldvariedasafunctionofhivestocking

density,weusedalinearmodelwiththecoefficientofvariation(standarddeviationof

yielddividedbythemean)asthedependentvariableandthehoneybeestockingdensityas

theindependentvariable.Separateregressionswereestimatedforsitesinhigh‐woodland

areasandlow‐woodlandareas.

Todeterminethedensityatwhichtheeffectofhoneybeesonyieldwassignificantly

greaterthanyieldwithnohives,weusedthepredictionequationtopredictyieldatagiven

hivedensity.Wevariedhives/hatoidentifytheloweststockingdensityatwhichtheupper

limitofthe95%confidenceintervalwithzerohives/hawaslessthanthelowerlimitofthe

95%confidenceinterval.AllstatisticalanalysiswasdoneusingJMPPro10(SASInstitute

Inc.2007).

2.0 Results

Cranberryyieldwas,onaverage,positivelyassociatedwiththenumberofhoney

beehives/ha(p<0.0001,Adj.R2=0.49,fig.1),butthisrelationshipvarieddependingonthe

amountofwoodlandinthesurroundinglandscape(hivesxlandscape,p=0.0091).Atfarms

withalowamountofwoodedhabitat(lessthanaverage,<41.6%)withina1kmradius,the

relationshipwasstrongandpositive(p<0.0001,Adj.R2=0.58),butatsiteswithahigh

amountofwoodedhabitat(aboveaverage,≥41.6%)within1km,therelationshipwasnot

significant(p=0.51,Adj.R2=0.25).Fromtheslopeoftheserelationships,wedetermined

thatthemarginalvalueofeachadditionalhivewas1098kg/hive(24.2bbl/hive)atlow‐

woodlandsitesand0kg/hive(nosignificantrelationship)athigh‐woodlandsites.

Variationincranberryyieldwasalsoeffectedbyhivedensity,butagain,onlyatsites

inlow‐woodlandlandscapes.Whentheproportionofwoodedhabitatishigh,increasing

hivedensityhasnoeffectonthecoefficientofvariation(CV,p=0.3088,Adj.R2=0.006,fig.

2).Whentheproportionofwoodedhabitatislow,increasinghivedensityresultsin

decreasedyieldCV(p=0.0392,Adj.R2=0.10).Theseresultssuggestthatgrowersathigh‐

woodlandsitesdonotgainanybenefitfromtheuseofhoneybeesbutgrowersatlow‐

woodlandsitesseeanincreaseinyieldandadecreaseinvariationbyusinghoneybees.

Theminimumnumberofhivesneededtorealizeasignificantyieldincreasewas4.2

hives/ha(1.7hives/ac)forsitesinlow‐woodlandlandscapes.Growersinhigh‐woodland

landscapesneverrealizedastatisticallysignificantyieldincreaseregardlessofthenumber

ofhives/haused.However,growersinahigh‐woodlandlandscapehadamarginallyhigher

yieldatzerohives/hathangrowersinalow‐woodlandlandscapeandallgrowershada

significantyieldatzerohives/ha(intercept,p<0.0001).Atzerohives/ha,yieldwas21.5

metrictons/ha(95%CI,19.1‐24.0)(192.4bbl/ac,95%CI,170.9–213.9)atlow‐woodland

sitesand25.3metrictons/ha(95%CI,22.6‐28)(226.2bbl/ac,95%CI202.2‐250.1)athigh‐

woodlandsites,whichrepresentsan18%increaseinyield.

Basedonthesedata,theeffectofvariationinhivestockingdensitydependsonthe

surroundinglandscape,however,anoptimalstockingdensity,thepointatwhichyieldis

maximized,couldnotbeestimatedsinceyieldscontinuetoincreasepasttheranges

reportedinthisstudyforfarmsinlow‐woodlandlandscapes.Wefoundnoevidenceof

yieldincreaseswiththeuseofhoneybeesatanyobservedstockingdensityforfarmssetin

high‐woodlandlandscapes.Wewereunabletodeterminetheoptimalhoneybeehive

stockingdensityforlow‐woodlandsitesbecausetherelationshipbetweenyieldand

hives/hadidnotreachapointofdiminishingreturns(fig.1).Therelationshipbetween

yieldandhives/haislinearfrom0hives/hato18.8hives/ha,thehigheststockingdensity

ofreportedbythegrowersforthetwelveyearsofdatareported.

3.0 Discussion

Individualcranberrygrowersspendtensofthousandsofdollarseachyearrenting

honeybeesforpollinationandstockingdensitiesvarywidely,suggestingthatgrowersmay

notbeoptimizingtheiruseofhoneybees.Bytakingadvantageofawealthofdataalready

heldbythegrowers,wewereabletoassembleapowerfuldatasetconsistingofmorethana

decadeofharvestdatafromnearly40differentmarshes.Thesedatarevealedthatyieldis

positivelyassociatedwithhivestockingdensity,butthatthisrelationshipdependsonthe

surroundinglandscape.Ourresultssuggestthatgrowerswhosemarshesaresetin

landscapeswithahighproportionofwoodlandmaybewastingmoneyonhoneybees,

whereincreasinghoneybeestockingdensitiesdidnotsignificantlyincreasecranberry

yield.Incontrast,atcurrentcranberrypricesandhivecosts,growerswhosemarshesare

setinlandscapeswithalowproportionofwoodlandshouldincreasetheirnetincomeby

usingahivestockingdensitygreaterthanthemaximumof18.8hives/ha(7.6hives/ac)

seeninourdata.Thisstudyprovidesthefirstrigorousassessmentofthevalueofhoney

beehivesforcranberryyieldthatweareawareof.

Themostobviouspatterninourdatasetwasthepositiverelationshipbetween

cranberryyieldandhives/hainsimplifiedlandscapes.Furthermore,formarshesinthese

low‐woodlandlandscapes,therelationshiphasnotreachedapointofdiminishingreturns,

suggestingthatgrowerscouldincreasestockingdensitiestoachievehigheryields.This

relationshipsupportstheuseofmanagedhoneybeesforcranberryyield,butalsosuggests

thatthepreviousrecommendationof4.9‐7.4hives/ha(2‐3hives/ac)requiresupdating.

Ourdatasuggestthatgrowersinlow‐woodlandlandscapescanincreasetheircranberry

yieldbyover1000kg/hiveforeachadditionalhoneybeehive/acused.Beyond18.8

hives/ha(7.6hives/ac),wecannotpredictwhatwillhappen.

Fromaneconomicperspective,cranberrygrowersappeartobebelowthemaximum

economicreturntheycouldachieveusingmanagedhoneybees.Growersinhigh‐woodland

landscapesusing10hives/hamaybewasting$700/ha($380/ac)whichonanaveraged

sizedmarshof32ha(80ac),amountsto$22,400/year.Inlow‐woodlandlandscapesatthe

stockingdensityreportedinourdata,however,theeconomicreturnsarestillincreasing

(BeattieandTaylor2009).Forthemosteconomicallyprofitablelevelofproduction,

growersshouldoperateatthepointwherediminishingreturnstoinputuseoccurs.A

recentstudyofblueberrypollinationfoundasimilarresultwithastronglinear

relationshipbetweenyieldandhivestockingdensity,suggestingthatblueberrygrowers

arealsonotmaximizingtheiruseofhoneybees(EatonandNams2012).

Economictheoryrecommendsincreasinguseofaninputuntilthemarketvalueofthe

additionalyieldgeneratedbytheadditionalinputjustequalsthecostoftheadditional

input.Atcurrentmarketpriceforcranberries($1.21/kgforcooperativeand$0.49/kgfor

independentgrowers,$65/bbland$22/bblrespectively)andhiverentalfees($70/hive),

theadditionofasinglehive/haprovidesan18:1returnoninvestmentsforcooperative

growersanda6.6:1returnoninvestmentsforindependentgrowersinlow‐woodland

landscapes.Withalinearresponseofyieldtohives/ha,growersinlow‐woodland

landscapeshavenotreachedtheeconomicallyoptimalhivestockingdensityandcould

continuetoincreasestockingdensityabovethemaximumof18.8hives/ha(7.6hives/ac)

reportedinthesedata.Theinteractingeffectofthelandscapealsosuggests,however,that

thereisnot,infact,asingleoptimalstockingdensityforcranberryindustry‐wide.

Theinteractionbetweenhivestockingdensityandsurroundinglandscapesuggeststhat

honeybeesarelesseffectiveatincreasingcranberrypollinationinhigh‐woodland

landscapes.Onepossibleexplanationforthisisthathoneybeesaremovingfromthecrop

intothenon‐cropinordertoaccessfloralresources.Vaissière(1990)foundthathoney

beeforagingdensitywasgreaterincottonfieldssurroundedby“poor”habitatwhichmay

explainthepatternseeninourstudyofahighercontributionofhoneybeestocranberry

pollinationinlow‐woodlandlandscapes.Pettisetal.(2013)furtherdemonstratedthat

honeybeesonaNewJerseycranberrymarshcollectedminimalamountsofcranberry

pollen,furthersupportingtheideathathoneybeesareforaginginnon‐crophabitats

surroundingthecranberrymarshes.

Anotherpatternevidentfromourdatasetisthatevenwhentherearenohivesofhoney

beespresent,growersstillachieveasignificantyield.Thiscouldbeduetoanumberof

factorsincludingferalhoneybees,nativebees,orothernon‐bioticvectorsofpollination.

Basedonadditionaldatacollectedbytheauthors,marsheswherehoneybeeswerenot

rentedhadveryfewifanyhoneybeespresent,nativebeeswerepresentinhighabundance

anddiversity(nearly200species)especiallyatmarshesinhigh‐woodlandlandscapes

(Gaineschapter3),andother,non‐bioticfactorscancontribute20‐80%oftotalcranberry

yield(Gaineschapter1).Previousstudieshavedemonstratedthatnativebeesareefficient

cranberrypollinators(CaneandSchiffhauer2003,Cariveauunpubl.data),suggestingthat

nativebeesmaybecontributingtothisyieldintheabsenceofhoneybees.Additionally,

assumingthatpollinationservicesalsoincreasewithnativebeeabundanceanddiversity,

thiscouldexplainwhythehigh‐woodlandmarsheswherenohoneybeesareusedhave

about20%greateryieldsthanlow‐woodlandsites,sincenativebeesarepositively

associatedwithnaturalhabitat(Rickettsetal.2008).

Despitethestrongandsignificantpatternsfoundinthisstudy,otherunmeasured

correlatesoflandusecouldcontributetotheobservedpatterns.Hivestockingdensitymay

becorrelatedwithothermanagementpracticesthatalsoaffectyield.Forexample,theuse

ofhighhoneybeestockingdensitiescouldalsobeassociatedwithmoreintensivefarming

practiceswithhigheroverallinputs(e.g.,fertilizer,pesticide,irrigation).Moredata

regardingmanagementpractices,suchastheapplicationoffertilizerorpesticides,

irrigation,andtheintensityofcropscoutingwhichmaybecorrelatedwithhivedensity

couldbeobtainedfromgrowers.Thesedatawouldallowfortheeffectofhivedensitytobe

disentangledfromothermanagementpractices.Finally,smaller‐scalefieldstudiesthat

experimentallyvarythehivestockingdensitycouldbeusedtoverifythepatternsobserved

inthishistoricaldataset.

Thisstudyrepresentsthefirstattempttodetermineeconomicallyoptimaluseofhoney

beesforcranberryproductionusingdatafromalargetimespanandacrossmanysites.

OurresultssuggestthattheoptimalstockingdensityhasnotbeenreachedonWisconsin

cranberrymarshesandfurtherresearchshouldexploreatwhatpointtheyieldresponse

curvereachesarateofdiminishingmarginalreturns.Ourresultsfurthersuggestthat

Wisconsincranberrygrowersinlow‐woodlandlandscapesshouldbeusingmorethan18.8

hives/ha(7.6hives/ac)tooptimizetheeconomicvalueofhoneybees.

Acknowledgements

Theauthorswouldliketothankallofthecranberrygrowerswhosharedtheiryieldand

honeybeerentalrecordswithus.ThisresearchwasfundedbyaHatchGrantawardedto

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Figurecaptions

Figure1:Cranberryyieldversushoneybeehivestockingdensity.Eachpointrepresentsa

singlemarshinasingleyear.Therewasastrongpositiverelationshipbetweenyieldand

hivestockingdensitybutonlywhenthepercentwoodlandinthesurroundinglandscape

waslow.

Figure2:Coefficientofvariationinyieldversushoneybeehivestockingdensity.Variation

inyielddecreasedwithincreasinghivestockingdensityatcranberrymarsheswherethe

surroundinglandscapewaslowinwoodland.Atmarshessetinhigh‐woodlandlandscapes,

therewasnorelationshipbetweenvariationinyieldandhivestockingdensity.

Hives/hectare

Figure 1

0 5 10 15 200

<41.6% woodland

≥41.6% woodland

Lowwoodland

Highwoodland (ns)

Lowwoodland

Highwoodland (ns)

0 5 10 15 200

Hives/hectare

nFigure 2

<41.6% woodland

≥41.6% woodland

CHAPTER3

Localandlandscapefactorsinfluencenativebees,yield,

andthecontributionofbeestoyield

Forsubmissionto:LandscapeEcology,BiologicalConservation,EcologicalApplications,

JournalofAppliedEcology

Abstract:Habitatlossandfragmentation,changesinlanduse,andintensivefarming

practicesareleadingcausesofbiodiversitylossaroundtheworld.Ofparticular

importanceinagroecosystemsisthelossofbeneficialinsectsthatprovideservicesto

farmersincludingpollination.Nativebeesprovidethemajorityofpollinationservicesin

somefarmingsystemsandhavethepotentialtoactasabufferagainstthecurrentdecline

inmanagedhoneybees.Inordertoensurethepersistenceofnativebeesandthe

pollinationservicestheyprovideinagroecosystems,itisimportanttounderstandhow

theyrespondtofeaturesofthesurroundinglandscapeandlocalfarmpractices.Therefore,

theobjectiveofthisstudywastodeterminetowhatextentnativebees,yield(ameasureof

pollinationsuccess),andthecontributionofbeestoyieldrespondtosurroundinghabitat

andlocalfactorsinaperennialcroppingsystem.Toaddressourobjective,wepan‐trapped

beesat49commerciallymanagedcranberrymarshesincentralWisconsinacrossa

landscapegradientfromhighlyagriculturaltohighlywooded.Yieldwasestimatedata

localfieldlevelandcollectedfromgrowersasamarsh‐wideaverage.Nativebee

abundanceandspeciesrichnesswerepositivelyassociatedwithopen,herbaceousand

woodedhabitat.Speciesrichnesswasalsopositivelycorrelatedtowoodededgedensity

andanindexoflocalpesticideuse.Yieldwaspositivelycorrelatedwithhoneybeehive

stockingdensityandcranberryfloraldensitybutwasnotassociatedwithnativebeesor

landscapefactors.Cagemanipulationstudiesweredoneatsitesalongalandscapegradient

andatsitesvaryinginlocalhoneybeeuse.Thecontributionofbeestocranberry

pollinationdidnotvaryasafunctionofsurroundinglandscapebutincreasedwith

cranberryfloweringuprightdensity.Theseresultssuggestthatbothlocalandlandscape

factorsareimportantpredictorsofbothnativebeeabundanceandrichnesswhilelocal

factorsaremoreimportantpredictorsofyieldandthecontributionofbeestoyield.Our

resultsdonotprovidestrongevidencethatnativebeesareastrongpredictorofyieldin

thissystem.

Keywords:nativebees,landscapeecology,EnvironmentalImpactQuotient,cranberry,

Vacciniummacrocarpon,structuralequationmodeling,lavaan

1.Introduction

Theexpansionofmodernagricultureandhumanactivityhaveledtothealterationand

fragmentationofthelandscapeanddestructionofnaturalhabitat.Agricultureiscurrently

thedominantland‐use,covering38%oftheterrestrialareaoftheglobe(Foleyetal.2005,

2011).Thislargescalealterationofthelandscapehasprofoundeffectsontheabilityof

organismstosurvive.Insectsareonegroupoforganismsthatprovidevaluableecosystem

servicesinagroecosystemssuchaspollination.Inordertofulfilltheirfeedingandnesting

resourcerequirements,manyofthesebeneficialinsectsmovebetweencropandnon‐crop

habitatsthroughouttheirlifecycle(Kremenetal.2007,Blitzeretal.2012).Becauseof

theirlimitedabilitytotravellongdistances(fromtensofmeterstoafewkilometers,

Zurbuchenetal.2010),theavailabilityofnon‐crophabitatwithintheagricultural

landscapeisofvitalimportance(Banaszak1992).

Althoughchangestothelandscapecanaffectthemovementandsurvivaloforganisms,

localfarmmanagementpracticescanalsohaveastronginfluenceonthepersistenceof

organismsinthearea,especiallythosewithlimitedflightdistancesthatmayexistprimarily

withinthefarmlandscape.Forexample,previousresearchhasshownthatfarmsthatuse

organicpracticesorhaveabundantfloweringnon‐cropplantssupportamorediverse

beneficialinsectcommunity(Bengtssonetal.2005,MorandinandKremen2013).

Additionally,thetiminganduseofpesticidescanhaveasignificantlethalorsub‐lethal

impactonbeneficialinsects(e.g.,bees,Desneuxetal.2007,Brittainetal.2010).Local

managementpractices,suchastillageandherbicideuse,affectthefloralandnesting

resourceavailabilityonthefarmwhichmaydirectlyaffectlocalscalepersistence.

Bees,onesuchexampleofmobileorganismsthatdeliverkeyservicestoagriculture

(Kremenetal.2007),arethemostimportantpollinatorsforcropproductionandare

sensitivetothecompositionandconfigurationofthelandscape,exposuretoagri‐

chemicals,andlocalresourceavailability(Pottsetal.2010).Historically,farmershave

reliedupononespecies,thenon‐nativehoneybee(Apismellifera),fortheirpollination

requirements.Inrecentyears,however,honeybeeshaveexperienceddrasticdeclinesasa

resultofmites,disease,andtherecentemergenceofColonyCollapseDisorder(CCD)(Ellis

etal.2010).Ashoneybeesdecline,farmerspayahigherpriceforhivesand,forsome

crops,mayneedtoseekalternativewaysofpollinatingtheircrops.

Nativebeesalsoprovidevaluablepollinationservices(LoseyandVaughan2006,

Winfreeetal.2008)andinsomesystemsareabletofullymeetthepollination

requirementsintheabsenceofhoneybees(watermelon,Winfreeetal.2008,cranberry,

MohrandKevan1987).Additionally,researchershavedemonstratedthatasnativebee

visitationincreases,cropyieldalsoincreasesregardlessofhoneybees(Garibaldietal.

2013).Byusingmanagementpracticesthatprotectorincreaseforageandnesting

resourcesfornativebees,farmersmayalsobeabletoincreasetheiryields.Although

farmersarenotlikelytoabandontheuseofhoneybeesforpollination,nativebeesmay

provideinsuranceagainstthedeclineinhoneybees(Winfreeetal.2007).Unfortunately,

declinesinnativebeepopulations(Pottsetal.2010,Cameronetal.2011)threatenthe

continuedprovisioningofthesepollinationservices,makingunderstandinghowlocaland

landscapefactorsinfluencenativebeepopulationsofgreatimportance.

Multiplestudieshavedocumentedthattheabundanceanddiversityofnativebees

increasewithproximitytonaturalhabitat(Kremenetal.2004,MorandinandWinston

2006)andareaswithdiversefloralresources(Pottsetal.2003,MorandinandKremen

2013).Currentresearchprovidesincreasingevidencethatthetypeandavailabilityof

habitatinthelandscape(i.e.,landscapecomposition)isimportantindeterminingnative

beeabundanceanddiversity.Arecentstudyprovidesevidencethatthearrangementof

habitat(i.e.landscapeconfiguration)isalsoimportant(Kennedyetal.2013).Fewstudies,

however,haveconsideredhowtheselandscapefactorsrelatetoyield(butseeRickettset

al.2004)orthecontributionofbeestoyield.Sinceyieldisauniversalmetricindicating

pollinationsuccess,understandinghowitrelatesdirectlyorindirectlytolocaland

landscapefactorscouldprovideinsightintofuturemanagementdecisionsinagro‐

ecosystems.

Inthisstudyweexaminedhownativebees,cropyield,andthecontributionof

nativeandmanagedbeestocropyieldvaryasafunctionoflocalandlandscapefeaturesin

theWisconsincranberryagro‐ecosystem.Previousstudieshaveshownthatnative,wild

beesareefficientcranberrypollinators(CaneandSchiffhauer2003)suggestingthattheir

conservationcouldprovideeconomicbenefitstocranberrygrowers.Theobjectivesofthis

studyweretodeterminetheinfluenceoflocalmanagementandlandscapefactorson(1)

nativebeeabundanceandspeciesrichness,(2)cranberryyield,and(3)thecontributionof

beestocranberryyield.Anunderstandingoftherelationshipsbetweenthesevariables

couldhaveimplicationsforfuturemanagementandconservationdecisions.

2.Methods

2.1StudySystemandSiteSelection

ThisstudywasconductedoncommercialcranberrymarshesincentralWisconsin

(USA),themaincranberrygrowingregioninthecountry.Thisregionisknownasthe

CentralSandPlainsandischaracterizedbysandysoilandflatopenterrain(DottandAttig

2004).Theareaisheavilyagriculturalandproducesmostofthestates’cranberryand

potatocrops.

Commercialcranberrymarshes(sites)wereselectedtospantheexistinglandscape

gradientfromhighlywoodedtohighlyagricultural(fig.1).Weuseddigitalorthophotosto

identifyallpossiblesitesandthencharacterizedthelandscapesurroundingeachsiteusing

remotelysensedland‐coverdata(USDA2011).Potentialsiteswereplottedonagraphof

percentwoodlandversuspercentagricultureandasubsetofthesesiteswerechosento

representtheentiregradient.Siteswereatleast2kmapartfromeachothertoensurea

minimumdegreeofspatialindependenceamongbeecommunities(Greenleafetal.2007,

Zurbuchenetal.2010).Wesampledat15sitesin2008,30sitesin2010,and20sitesin

2011foracombined49uniquesites(i.e.somesitesweresampledmultipleyears).

Samplingtookplaceinacornerofthemarshclosesttonon‐crophabitat.Eachmarshis

composedofagroupofindividualbeds(~40mx200m)andsamplingwasdonewithinthe

cornerbedandthebedimmediatelyadjacenttoit.

2.2Localvariables

Todeterminecranberryfloraldensity,flowerswithintenrandomlyplaced1ft2

quadratspersitewerecountedduringpeakbloomin2010and2011.

Localpesticidetoxicityscoreswerecalculatedforeachsitebasedonpesticidespray

recordscollectedfromthegrowersforeachsamplingyear.Weusedamodifiedversionof

theEnvironmentalImpactQuotientofPesticidesFieldScore(Kovachetal.1992)which

simplifiessprayrecordstoasingleindexbasedonavarietyoffactorsincludingtoxicitytoa

targetorganism,activeingredients,andthenumberofapplicationsmade.

mEIQ=∑(Z*P*3)(%activeingredient/100)(applicationrate)(#ofapplications)

whereZ=beetoxicity

andP=plantsurfacehalf‐life

Whenanapplicationratewasnotindicatedonsprayrecords,theraterecommendedonthe

materiallabelwasused.ThepercentactiveingredientwasextractedfromtheMaterial

SafetyDataSheet(MSDS)foreachchemical.Whenratewasinpounds/acre,onepound

wasconsidered16oz.

2.3Landscapevariables

Todescribethelandscapearoundeachsite,wecalculatedbothcompositionand

configurationmetricsusingPatchAnalyst4(Rempeletal.2008)inArcGIS10(ESRI2011).

Thecompositionprovidesanindexofhabitatandresourceavailabilitywhileconfiguration

describestheaccessibilityofthathabitattoorganismsinthelandscape.Forcomposition

(i.e.percentcover),wenarrowedtheoriginal56CDLland‐covercategoriesdownto14

categorieswhichrepresentedatleast1%ofthetotallandareawithin1kmofallsites.

These14categoriescombinedrepresent96.4%oftheland‐coverwithin1kmofallsites.

Tofurthersimplifythelandscapecompositiontojusttwoaxes,weperformedaPrinciple

ComponentsAnalysis(PCA)usingthe14categories(fig.2).ThePCAvaluesforaxis1and

axis2werethenusedinourstatisticalanalysistorepresentlandscapecomposition.

Landscapeconfigurationwasrepresentedbywoodededgedensity(i.e.lengthofwooded

edgeswithin1km).Woodededgesareexpectedtoprovidegoodbeehabitatwithaccessto

multiplehabitattypes(woodlandandopen/agriculture)andcreateauniquehabitattype

withanabundanceofnestingandforagingresources(Diaz‐Foreroetal.2013).

2.4Nativebeeabundanceandspeciesrichness

Tomeasurenativebeeabundanceandspeciesrichness,wepantrappedspecimens

fromMaytoAugustof2008,2010,and2011.Eachyear,samplesweretakenbefore,during

andaftercranberrybloom.Pantrapswerefilledwithsoapywaterandsetdowninthe

cranberryvinesintwoparalleltransectslocatedeitherimmediatelyadjacenttoanon‐crop

marshedgeor50metersawayfromtheedge.Thedecisiontolocatethetransectsneara

non‐farmedgewasbasedonresearchindicatingthatbeesrespondpositivelytoproximity

tonaturalhabitat(reviewedbyRickettsetal.2008),soiftherewereanyresponsebybees

tolandscape,itwouldbecapturedinourstudydesign.Eachtransectincluded5setsof

threepantraps(blue,yellow,andwhite,ACEFluorescentspraypaint)setat10mintervals.

Specifictrappingmethodsvariedslightlyfromyeartoyear.In2008,trapswere

madefrom5ozplasticbowls(Chinettebrand).Trapswereleftineachmarshfor6‐hour

intervalsbetween8amand4pmandallsiteswerevisitedwithinthreedays(5sitesper

day).Datawereonlycollectedondaysdeemedtobegoodbeedays(windbelow2.5m/s,

temperatureabove15oC,skyconditionssunnytobrightovercast).In2010and2011,traps

weremadefrom12ozplasticcups.Trapswereleftineachmarshfor3‐dayintervalsand

allsiteswerevisitedwithintwodays(~15sitesperday).

Specimenswerestoredinto70%alcoholthendried,pinned,labeled,andsortedto

morphospeciesinthelabbeforebeingsenttoataxonomistforspecieslevelidentification.

2.5Yield

Yielddatawascollectedbothempiricallyonasmallplotscaleinthefieldandata

marsh‐widescalefromgrowers.Toestimatetheplotlevelyield,four1ft2berrysamples

weretakenfromeachsiteduringthe2011fieldseason.Thismethodisusedbycropscouts

andfarmerstoestimateyieldbeforeharvest(J.Sojka,pers.comm.).Allberrieswithin

randomlyselected1ft2quadratswereharvestedinlateSeptemberbeforecranberry

harvestandweighedinthelab.Wetweightwasusedasthisiseasilyconvertedtothe

industrystandardyieldmetricofbarrels/acre(1bbl=100lbs).

Todeterminethedirecteffectsoflocalandlandscapeeffectsonnativebee

abundanceandspeciesrichnessandthedirectandindirecteffectsonyield,weusedpath

analysiswhichisaformofStructuralEquationModeling(SEM).SEMisausefulwayto

analyzecomplex,multivariatelinearrelationships,intercorrelationofpredictors,and

providesamethodtoallowseparationofdirectandindirecteffects(Grace2006).Fordata

collectedattheplotlevel(n=17),thesmallnumberofvariablesandpathswaslimitedby

oursamplesize.Incontrast,ourmarsh‐widedatahadfarmoreobservations(n=42)

allowingustoincludemorevariablesandpathsinourmodel.Ourhypothesizedmodelfor

ourestimatedplotlevelyieldincludeddirecteffectsofhoneybeehivestockingdensity,

nativebeeabundance,andnativebeerichnessonyield;directeffectsofPC1,PC2,and

woodededgedensityonnativebeeabundanceandspeciesrichness;andindirecteffectsof

PC1,PC2,andwoodededgedensityonyield(fig.3).Ourhypothesizedmodelforthe

marsh‐wideaverageyieldincludeddirecteffectsofhoneybeehivestockingdensity,

cranberryfloraldensity,mEIQ,nativebeeabundanceandnativebeespeciesrichnesson

yield;directeffectsofmEIQ,cranberryfloraldensity,woodededgedensity,PC1,andPC2

onnativebeeabundanceandspeciesrichness;andindirecteffectsofmEIQ,PC1,PC2,and

woodededgedensityonyield(fig.4).Alllocalandlandscapevariablesusedinboth

modelswerefromthesamedata.Inordertodetermineindirecteffects,wemultipliedthe

standardizedcoefficientsofdirecteffects(Mattesonetal.2013).Aχ2goodnessoffittest

wasusedtodeterminewhetherthemodelwasagoodfitofthedata.AllSEManalysiswas

doneusingtheLavaanpackage(Rosseel2012)inRStudio0.97.551(RStudio2012).

2.6Contributionofbeestoyield

Todeterminehowthecontributionofbeestocranberrypollinationvariesasa

functionoflocalorlandscapefactors,wedidcagemanipulationstudiesin2011and2012.

Cageswere50cmx50cmandwerecoveredwithnylontulletoexcludepollinators.Cages

weresetupbeforecranberrybloomandremovedoncebloomwascomplete.Allberries

withina1ft2areainthecenterofthecagesandinseparateopenplotswereharvestedin

lateSeptemberandcountedandweighed(wet)toestimateyield.In2011,3cages/site

wereestablishedat30sites(n=90cages)alongalandscapegradientofhighwoodedto

highagriculture.In2012,10cages/sitewereestablishedat11sites(n=110cages),5of

whichhadhoneybeespresentand6absent.Allsitesin2012werelocatedinhighwooded

landscapestocontrolforlandscapeeffectsonnativebeesoryield.

Todeterminewhetherthecontributionofbeestoyieldvariesasafunctionoflocal

andlandscapefactors,wedidamultipleregressiononyieldwithcagetreatment,local,and

landscapefactorsaspredictorvariables.Forour2011cagemanipulationacrossa

landscapegradient,ourpredictorvariablesincludedcagetreatment,PC1,PC2,cage*PC1,

andcage*PC2aspredictorvariablesandsiteasarandomterm.Tounderstandthe

influenceoflocaleffects,wedidamultipleregressiononouryielddatacollectedinour

2012cagemanipulationstudythatwasonfarmssetinhighwoodlandlandscapesonly.

Ourpredictorvariablesincludedcagetreatment,honeybeehivestockingdensity,native

beeabundance,densityofcranberryfloweringuprights,cage*honeybees,cage*nativebee

abundance,cage*uprightdensity,andfarmsiteasarandomterm.Thisanalysiswasdone

usingJMP10.0.0(SASInstituteInc.2007).

3.Results

Wecollectedatotalof6673specimensrepresenting182speciesofbeesoverthree

fieldseasons(Appendix3.1).TheseincludeseveralnewrecordsforthestateofWisconsin

includingCoelioxysimmaculata,Lasioglossumlusorium,Megachileaddenda,andXenoglossa

kansensisaswellas19specimensofBombusterricola,aspeciesbelievedtobeindecline

throughouttheMidwesternUnitedStates(Cameronetal.2011).Overallthemost

abundantspeciescollectedwereLasioglossumadmirandum(n=523representing8%ofthe

totalsample),Agapostemontexanus(n=425,6%),andLasioglossumpilosum(n=367,5%).

ThesedatarepresentanexpandedspecieslistandspeciesrangesforWisconsin(Wolfand

Ascher2008)andprovideacomprehensivelistofbeespeciesfoundintheWisconsin

cranberrysystem.

3.1PrincipleComponentsAnalysisonlandscape

OurPCAindicatedastronggradientoflandcoverfromwoodedhabitattorowcrop

agriculture(e.g.,corn,soybeans)(PC1,26.1%)andfromwetlandandcranberrytoopen,

herbaceousandwoodedhabitat(PC2,15.8%)(fig.2).Becauseofthewaterrequirements

forcranberryproductionandthehistoricpracticeofmanagingnaturalwetlandsfor

cranberryproduction,cranberrymarshes,herbaceouswetland,andopenwaterwere

clusteredtogether.

3.2Beeabundance,speciesrichness,andyield

3.2.1Modelbasedonmarshlevelestimates

Ourmodelbasedoncranberryyieldasreportedbygrowersatthemarshlevel

foundastrongpositivecorrelationbetweennativebeeabundanceandopen,herbaceous

andwoodedhabitatinthelandscape(PC2,R2=0.30,standardizedpathcoefficient=0.52,

p<0.001,fig.3).Therewasalsoamarginallysignificantpositiveassociationbetweenbee

abundanceandlocalpesticideintensity(mEIQ,standardizedpathcoefficient=0.25,

p=0.06).Beespeciesrichnesswasalsoassociatedwithbothlandscapecharacteristicsand

localfactors.Open,herbaceousandwoodedhabitatinthelandscapehadastrongpositive

associationwithnativebeespeciesrichness(PC2,R2=0.45,standardizedpathcoefficient=

0.61,p<0.001).Localpesticideintensityalsohadapositiveassociationwithbeespecies

richness,possiblyasaresultofacorrelationbetweensprayintensityandbee‐friendly

managementpracticessuchastheuseoflesstoxicchemicals(mEIQ,standardizedpath

coefficient=0.32,p=0.005).Cranberryfloraldensityhadamarginallysignificant,weak

negativeassociationwithnativebeespeciesrichness(standardizedpathcoefficient=‐0.11,

p=0.11).

Cranberryyieldasmeasuredatthemarshscalewasdirectly,positivelycorrelated

withhoneybeehivestockingdensity(R2=0.56,standardizedpathcoefficient=0.65,

p<0.001)andmarginallywithcranberryfloraldensity(standardizedpathcoefficient=

0.18,p=0.13).Therewerenoindirecteffectsoflandscapeonyield.The∆AICbetweenthe

hypothesizedmodelandourfinalmodelwas12.64.Anon‐significantχ2goodnessoffittest

indicatedthatourmodelwasagoodfit(p=0.62).

3.2.2Modelbasedonplotlevelestimates

Nativebeeabundancewasstronglycorrelatedwithincreasingwoodedandopen,

herbaceoushabitatinthesurroundinglandscape(PC2,R2=0.43,standardizedpath

coefficient=0.66,p<0.001,fig.4)butnotwithanylocalvariables.Nativebeespecies

richnesswasalsostronglycorrelatedwithincreasingwoodedandopen,herbaceous

habitat(PC2,R2=0.46,standardizedpathcoefficient=0.52,p=0.002),aswellasthelength

ofwoodededgesinthelandscape(woodededgedensity,standardizedpathcoefficient=

0.25,p=0.014).Richnesswasnotassociatedwithlocalfactors.

Cranberryyieldasmeasuredattheplotscalewasstronglyassociatedwithlocal

factorsbutonlymarginallywithlandscapefactors.Therewasadirect,positiveassociation

betweenyieldandhoneybeehivestockingdensity(R2=0.32,standardizedpathcoefficient

=0.43,p=0.02).Yieldwasmarginally,negativelyassociatedwithnativebeeabundance

(standardizedpathcoefficient=‐0.36,p=0.054)andindirectly,negativelywithincreasing

woodedandopen,herbaceoushabitatinthelandscape(PC2,standardizedpathcoefficient

=‐0.24).The∆AICbetweenthehypothesizedmodelandourfinalmodelwas7.84.Anon‐

significantχ2goodnessoffittestindicatedthatourmodelwasagoodfit(p=0.81).

3.3Contributionofbeestoyield

Excludingbeeshadasignificanteffectonyield,asdidthesurroundinglandscape.

Fromour2011cagemanipulationalongalandscapegradient,wefoundthatexcluding

pollinators(cage,p=0.0012,F1,25=14.0)andincreasingwoodlandinthesurrounding

landscape(PC2,p=0.0165,F1,25=6.6,fig.5)hadsignificantnegativeeffectsonyield.The

effectofexcludingbeeshadthesameeffectwhetherwoodlandinthesurrounding

landscapewashighorlow(cage*PC2,p=0.12,F1,25=2.6).

Whenwehadfinescalecranberryfloraldensitydata,wefoundthatfloraldensity

andthepollinatorexclusionhadaninteractingeffectonthecontributionofbeestoyield.

Theresultsofour2012cagemanipulationindicatethatthemostimportantfactors

affectingyieldwerepollinatorexclusion(cage,p<0.0001,F1,9=58.3),floweringupright

density(p<0.0001,F1,9=96.6),andtheirinteraction(p=0.0051,F1,9=13.5),indicatingthat

thecontributionbybeesisdifferentwhenfloraldensityishighcomparedtolow(fig.6).

4.Discussion

Previousresearchhasinvestigatedtheinfluenceoflocalandlandscapefactorson

nativebeeabundanceandspeciesrichness,butfewhaveconsideredhowthesefactors

influenceyieldorthecontributionofbeestoyield.Inthisstudy,wefoundthatnativebees

respondstronglytolandscapefactors(i.e.,open,herbaceousandwoodedhabitat)but

weaklytolocalmanagement(i.e.,sprayintensity,cranberryfloraldensity).Cranberry

yield,incontrast,respondsstronglytolocalmanagement(i.e.,honeybeehivedensity,

cranberryfloraldensity)butweaklytolandscapefactorsandnativebees.Thecontribution

ofnativeandmanagedbeestocranberryyieldwasinfluencedbylocalfactors(i.e.,

cranberryfloraldensity)butnotlandscapefactors.Asthedensityofcropflowers

increased,thecontributionofbeesalsoincreased.Theseresultssuggestthat,atleastin

thissystem,theeffectoflocalmanagementonyieldismuchstrongerthanthatofthe

landscape.Wefoundnoevidencethatnativebeescontributetocranberryyield.

Theclearestpatternfromourstudywasthepositiveinfluenceofwoodlandon

nativebees.Bothnativebeeabundanceandspeciesrichnesswerestronglyassociatedwith

increasingwoodlandinthesurroundinglandscape.Thissupportspreviousstudies

showingthatbeesrespondpositivelytonaturalhabitatinthesurroundinglandscape

(reviewedbyRickettsetal.2008,Kennedyetal.2013).Thispatternislikelyduetothefact

thatnaturalhabitatsprovideforageandnestingresourcesthroughouttheseason,whereas

agriculturallandwithfloweringcrops,likecranberry,onlyprovideforageresourcesfora

veryshorttimespan.Wealsofoundapositiveinfluenceofwoodededgedensityonspecies

richness.Woodededgeslikelyprovidegoodnestingsitesforstem,ground,andcavity

nestingbeesincloseproximitytoopenhabitatswhereforageresourcescouldbeabundant.

Thepositiverelationshipbetweenlocalpesticideintensity(i.e.,mEIQ)andnative

beespeciesrichnesswasunexpected.Wehypothesizedthatlocalpesticidesprayintensity

wouldbenegativelyassociatedwithnativebeessincemoreexposuretopesticidesshould

haveadetrimentaleffectonbees(Desneuxetal.2007,Brittainetal.2010).Onepossibility

isthatsummarizingsprayintoasingleindexisaninadequatemethodforrepresenting

actualsprayexposure.Previousstudiesthatusedsprayindicesasanindexofpesticideuse

havealsofoundunexpected(Cramptonetal.2010),inconsistent(Singleton2010),orno

effects(JenkinsandIsaacs2007)ofsprayindexonbeneficialinsectssuggestingthatthis

maybethecase.Anotherpossibilityisthatahighsprayindexratingiscorrelatedwith

otherbee‐consciouspracticessuchassprayingatnightorusinglessharmfulspraysduring

bloom.Evenifgrowersspraymoreoftenoruseharsherchemicals,whenandhowthey

applythechemicalswillhaveabiginfluenceonhowitaffectsbeneficialinsects.Wisconsin

cranberrygrowershaveadocumentedrecordoffollowingenvironmentallyconscious

managementdecisions(ColquhounandJohnson2010)soitmightbeexpectedthatthey

wouldfollowpollinator‐consciouspracticesaswell.

Anotherclearpatterninourstudywasthestrongrelationshipbetweencranberry

yieldandhoneybeestockingdensity,butthelackofassociationbetweenyieldandnative

beeabundance.Whilethereisastrongrelationshipbetweencranberryyieldandhive

stockingdensity(Gaines,chp.2),thepatternheremaypartlybeanartifactofscale.The

associationbetweenyieldandhoneybeehivestockingdensitywasstrongerinourmodel

basedonthemarsh‐wideyieldestimatesthaninourmodelbasedonplotscaleyield

estimates.Notsurprisingly,honeybeehivestockingdensitywerealsobasedonmarsh‐

wideaveragesprovidedbythegrowers,whereasnativebeeabundancewasbasedonaplot

levelsampletakeninthesameareaofthemarshastheplotscaleyieldestimates.

Additionally,honeybeehivesareoftendispersedacrosstheentiremarshwhereasnative

beeabundancedecreasestowardsthecenterofthemarshandawayfromanon‐cropfarm

edge(Gaines,unpubl.data).Thismayallowhoneybeestohaveamoreeveninfluenceon

marsh‐wideyield,whereasthenativebeeswouldhaveastrongerinfluenceattheedgeof

themarsh(EvansandSpivak2006).

Thelackofinfluenceoflandscapeonthecontributionofbeestocranberryyieldwas

surprising.Weexpectedthatthecontributionbybeeswouldincreasewithincreasing

woodlandinthesurroundinglandscapebecausetherewouldbeagreaterabundanceand

richnessofbeespresent.Furthermore,previousstudieshavefoundapositiveinfluenceof

naturalhabitatoncropyield(Ricketts2004,MorandinandWinston2006).Instead,we

foundthatyielddecreasedaswoodedandopen,herbaceoushabitatinthelandscape

increasedandthatthecontributionofbeestoyielddidnotchange.Thispatternsuggests

eitherthatthenativebeesarenotcontributingtocranberryyieldorthatthecontribution

oflocalhoneybeesmasksanycontributionbynativebees.

Despitealackofinfluenceofthelandscapeonbeecontributionstoyield,thelocal

factorcranberryfloraldensitywasanimportantpredictorofthecontributionbybeesto

yield.Asfloraldensityincreased,thecontributionbybeesalsoincreased.Beesare

attractedtolargefloraldisplays,soincreasingthedensityofflowersmaymakethe

cranberrymarshmoreattractivetobees.Alternatively,floraldensitymaybecorrelated

withothermanagementpracticessuchashigherhoneybeehivestockingdensitiesand

moreintensivepracticesthatareassociatedwithincreasedyield.

Theresultsofthisstudysuggestthatlocalfarmmanagement,includingtheuseof

managedbees,hasastrongeffectoncropyield.Althoughwefoundnoevidencethatnative

beesarecontributingtothepollinationofcommercialcranberry,someWisconsin

cranberrygrowersdonotusemanagedhoneybeesforpollination,suggestingthatthe

nativebeesdocontribute.Futureresearchshouldconsideralternativemethodsfor

determiningthecontributionofnativebeestoyield.

Acknowledgements

Wewouldliketoespeciallythankallofthecranberrygrowerswhoallowedusto

conductresearchontheirfarmsandwhoprovidedyielddatatous.Wecouldnothave

collectedandprocessedallofourdatawithoutthehelpofmanyfieldandlabassistants:

EmilyFricke,AdamHiggins,CarlKaiser,MerrittSingleton,AllisonDehnel,Collin

Schwantes,BrianHedberg,AmandaRudie,ChaseFritz,MollyWaytes,GavinJones,Federica

Lacasella,JuliaTiede,RachelMallinger,andAliNelson.JayneSojkaandDanMahrassisted

withinitialsiteselection.BeeidentificationwasverifiedbyMikeArduser,JasonGibbs,and

JohnAscher.StatisticalassistancewasprovidedbyBrianSpiesmanandTaniaKim.This

researchwasfundedbyaHatchGrantawardedtoCG.

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Figurecaptions

Figure1:Thedistributionofcranberrymarshes(sites)alongalandscapegradientof

woodedhabitatandagriculture.Siteswerechosentospanasmuchofthegradientas

possible.

Figure2:APrincipleComponentsAnalysisshowingtherelationshipbetweenlandcover

typessurroundingoursites.Eachlandcovertyperepresentsatleast1%ofthetotalarea

withina1kmradiusofallsites.

Figure3:Hypothesized(gray)andfinal(black)structuralequationmodelexplainingnative

beeabundance,speciesrichness,andthemarsh‐wideaveragecranberryyield.Gray

arrowsindicateconnectionsthatwereremovedfromthemodel.Solidblackarrows

indicatepositiverelationshipswhiledashedarrowsindicatenegativerelationships.

Numbersadjacenttoarrowsarestandardizedregressioncoefficientsalongwiththeir

significance(*).Thecoefficientindicatesthestrengthoftherelationship.

Figure4:Hypothesized(gray)andfinal(black)structuralequationmodelexplainingnative

beeabundance,speciesrichness,andfieldestimatedcranberryyield.Grayarrowsindicate

pathsthatwereremovedfromthemodel.Solidblackarrowsindicatepositive

relationshipswhiledashedarrowsindicatenegativerelationships.Numbersadjacentto

arrowsarestandardizedregressioncoefficientsalongwiththeirsignificance(*).The

coefficientindicatesthestrengthoftherelationship.

Figure5:Yieldfromthe2011cagemanipulationexperimentacrossalandscapegradient

wasbestestimatedbyamodelthatincludedcagetreatmentandprinciplecomponent2.

Thecontributionofbeestoyielddoesnotvaryasafunctionofthelandscapeasindicated

byanon‐significantinteractionterm(cage*PC2,p=0.12).

Figure6:Yieldfromthe2012cagemanipulationexperimentwasbestestimatedbya

modelthatincludedcagetreatment,thedensityoffruitinguprightsandtheirinteraction

(cage*uprights,p=0.0054),indicatingthattheinfluenceofinsectpollinatorsonyieldis

greaterwhenthedensityoffloweringuprightsishigher.

Figure 1

Agriculture within 1km (%)

0 10 20 30 40 50 60 70 800

Figure 2

CORNPASTURE/HAY

SOYBEANSALFALFA

PASTURE/GRASS

CRANBERRYMARSH

DEVELOPED/OPEN SPACE

OPENWATER

HERBACEOUSGRASSLAND

HERBACEOUSWETLAND

WOODEDWETLAND

MIXED FOREST

EVERGREENFOREST

DECIDUOUSFOREST

-1.0 -0.5 0.0 0.5 1.0

Component 1 (26.1 %)

Cranberry

Honey beehives/acre

Native BeeAbundance

Native BeeRichness

Cranberry yield(marsh avg.)

Figure 3

Removed path

0.65***

0.61***

0.52***

0.32**

R2=0.30

R2=0.45

R2=0.56

0.80***

† p<0.10** p<0.01*** p<0.001

wood edge density

0.25†

tMarsh Scale Model

Honey beeabundance

Native BeeAbundance

Native BeeRichness

Cranberry yield(estimate)

Figure 4

Removed path

† p<0.10* p<0.05** p<0.01*** p<0.001

-0.36†

0.52**

0.66***

R2=0.43

R2=0.46

R2=0.32

0.85**

wood edge density

Plot Scale Model

Figure 5

-5 -4 -3 -2 -1 0 321

Principle Component 2 (PC2)

Fruiting uprights/36 sq. in.

0 10 20 30 40 50 60 70 80

Figure 6

Appendix3.1:ListofbeespeciesandtheirabundancescollectedinWisconsincranberrybetween2008and2011.SpecimenidentificationwasverifiedbyMikeArduser,JohnAscher,andJasonGibbs.

Species 2008 2010 2011 TOTAL

Agapostemon sericeus 33 80 38 151

Agapostemon splendens 6 38 54 98

Agapostemon texanus 173 131 121 425

Agapostemon texanus or splendens 1 1

Agapostemon virescens 19 117 125 261

Andrena (Ptilandrena) erigeniae 9 9

Andrena (Trachandrena) sp. 1 2 2

Andrena alleghaniensis 3 1 1 5

Andrena arabis 1 1 2

Andrena barbilabris 5 1 6

Andrena carlini 20 13 1 34

Andrena carolina 2 2

Andrena ceanothi 7 1 8

Andrena chromotricha 1 1

Andrena commoda 1 2 3 6

Andrena crataegi 1 5 2 8

Andrena cressonii 17 16 4 37

Andrena distans 1 2 3

Andrena erythrogaster 1 1

Andrena forbesii 2 2

Andrena fragilis (cf) 1 1

Andrena hippotes 1 1

Andrena imitatrix 1 1

Andrena krigiana 1 1

Andrena milwaukeensis 1 1

Andrena miranda 2 4 4 10

Andrena miserabilis 4 1 1 6

Andrena nasonii 1 4 5

Andrena nivalis 11 164 28 203

Andrena nr dunningi 1 1

Andrena perplexa 1 1 4 6

Andrena platyparia 2 2

Andrena rufosignata 3 3

Andrena rugosa 1 1

Andrena sigmundi 2 2

Andrena vicina 11 9 3 23

Andrena violae 1 1

Andrena wilkella 5 8 2 15

Andrena wilmattae 1 1

Andrena w‐scripta 2 2

Anthophora terminalis 5 10 15

Augochlora pura 2 1 1 4

Augochlorella aurata 14 65 79 158

Augochloropsis fulgida 13 13

Augochloropsis metallica 5 9 14

Augochloropsis sumptuosa 1 1 2

Bombus auricomus 1 1

Bombus bimaculatus 1 24 13 38

Bombus borealis 4 12 8 24

Bombus fernalde 2 2

Bombus fervidus 1 6 11 18

Bombus griseocollis 5 25 18 48

Bombus impatiens 5 90 35 130

Bombus pensylvanicus 1 1

Bombus rufocinctus 5 1 6

Bombus sandersoni 6 4 10

Bombus sp. 1 1

Bombus ternarius 5 56 79 140

Bombus terricola 17 2 19

Bombus vagans 2 13 18 33

Calliopsis andreniformis 3 3

Ceratina calcarata 1 1

Ceratina calcarata or dupla or micmaqi 1 1

Ceratina dupla 1 1

Ceratina dupla or calcarata 8 8

Ceratina sp. 3 3

Coelioxys immaculata* 2 1 3

Colletes inaequalis 20 20

Dufourea monardae 3 3

Eucera atriventris 1 1

Eucera hamata 26 60 86

Halictus confusus 73 66 49 188

Halictus ligatus 6 71 40 117

Halictus parallelus 19 8 27

Halictus rubicundus 8 11 8 27

Hoplitis pilosifrons 2 2 1 5

Hoplitis producta 4 1 5

Hoplitis spoliata 3 1 4

Hoplitis truncata 1 1

Hylaeus (Prosopis) nr modestus 2 2

Hylaeus affinis/modestus 2 2

Hylaeus basalis 1 1

Hylaeus mesillae 2 1 3 6

Hylaeus modestus 1 1

Lasioglossum (Dialictus) lineatulum 17 85 30 132

Lasioglossum (Dialictus) MA WI sp. A 128 128

Lasioglossum (Dialictus) MA WI sp. B 99 99

Lasioglossum (Dialictus) MA WI sp. D 12 12

Lasioglossum (Dialictus) MA WI sp. E 1 1

Lasioglossum (Dialictus) MA WI sp. F 1 1

Lasioglossum (Dialictus) MA WI sp. G 1 1

Lasioglossum (Dialictus) MA WI sp. H 1 1

Lasioglossum (Dialictus) nr MA WI sp. B 3 3

Lasioglossum (Dialictus) perpunctatum 5 9 3 17

Lasioglossum (Dialictus) pilosum 66 215 86 367

Lasioglossum (Dialictus) rohweri 53 53

Lasioglossum (Dialictus) sp. 3 3

Lasioglossum (Dialictus) viereckii 5 2 7

Lasioglossum (Dialictus) zephyrum 40 46 4 90

Lasioglossum ?unknown 1 1

Lasioglossum acuminatum 70 131 33 234

Lasioglossum admirandum 392 131 523

Lasioglossum albipenne 3 10 5 18

Lasioglossum anomalum 1 1

Lasioglossum athabascense 1 13 1 15

Lasioglossum bruneri 12 22 13 47

Lasioglossum cf. floridanum 1 1

Lasioglossum cinctipes 7 13 6 26

Lasioglossum coreopsis 1 1

Lasioglossum coriaceum 32 149 119 300

Lasioglossum cressonii 4 11 12 27

Lasioglossum ellisiae 1 2 3

Lasioglossum ephialtum 18 18

Lasioglossum fedorense 32 4 36

Lasioglossum floridanum 1 1

Lasioglossum forbesii 1 1 2

Lasioglossum forbesii or paraforbesii 1 1

Lasioglossum foxii 1 1

Lasioglossum heterognathum 1 1

Lasioglossum laevissimum 2 2

Lasioglossum leucocomum 127 73 200

Lasioglossum leucozonium 30 265 66 361

Lasioglossum lusorium* 1 1

Lasioglossum lustrans 1 29 3 33

Lasioglossum lustrans (3 cells) 2 2

Lasioglossum michiganense 1 1

Lasioglossum mitchelli 3 1 4

Lasioglossum nelumbonis 6 40 46 92

Lasioglossum nigroviride 1 2 3

Lasioglossum novascotiae 1 1

Lasioglossum nymphaearum 31 85 116

Lasioglossum oblongum 7 1 8

Lasioglossum oceanicum 121 121

Lasioglossum paraforbesii 5 47 9 61

Lasioglossum pectorale 16 52 54 122

Lasioglossum pictum 1 1

Lasioglossum pruinosum 1 1

Lasioglossum smilacina 4 4

Lasioglossum sp. 1 1

Lasioglossum subviridatum 16 1 17

Lasioglossum swenki 1 17 34 52

Lasioglossum taylorae 2 2

Lasioglossum timothyi 2 1 3

Lasioglossum versatum 95 25 120

Lasioglossum viridatum 8 11 19

Lasioglossum weemsi 2 2

Lasioglossum zonulum 30 105 102 237

Macropis nuda 1 1 1 3

Megachile addenda* 11 21 7 39

Megachile brevis 2 2 4

Megachile gemula 7 6 1 14

Megachile latimanus 5 17 22

Megachile latimus 21 21

Megachile relativa 1 1 2

Melissodes (Eumelissodes) sp. 9 9

Melissodes agilis 10 10

Melissodes bimaculata 15 8 23

Melissodes desponsa 1 11 19 31

Melissodes druriella 20 20

Melissodes subillata 3 3

Melissodes trinodis 6 6

Melissodes agilis or trinodis 14 14

Nomada sp. 3 3

Nomada sp. 1 1 1

Osmia albiventris 1 1

Osmia atriventris 1 2 3

Osmia distincta 9 7 2 18

Osmia georgica 2 2

Osmia inspurgens 6 6

Osmia lignaria 1 1 2

Osmia pumila 21 5 1 27

Osmia simillima 1 3 4

Osmia tersula 2 1 3

Osmia virga 1 1

Peponapis pruinosa 6 8 14

Perdita maculigera 1 1

Pseudopanurgus helianth 1 1

Psithyrus sp. 4 4

Sphecodes atlantis 1 1 2

Sphecodes confertus 2 2

Sphecodes coromus 1 1

Sphecodes davisii 2 1 3

Sphecodes dichrous 6 6

Sphecodes levis 1 1

Sphecodes mandibularis 1 1 2

Sphecodes rannacali 2 2

Sphecodes solonis 1 1

Stelis (Stelis) labiata 1 1

Stelis foederalis? 1 1

Tripeolis sp. 1 1

Xenoglossa kansensis* 11 5 16

*indicates new record for the state of Wisconsin

CHAPTER4

Understandingthebarrierstoimplementationofon‐farmhabitatconservationof

nativebeesinWisconsincranberry

Forsubmissionto:JournalofInsectConservation

Abstract:Theexpansionofmodernagriculturehasledtothelossandfragmentationof

naturalhabitat,resultinginaglobaldeclineinbiodiversity.Onewaytomitigatethe

negativeeffectsofagricultureonbiodiversityisthroughtheconservationofnaturalhabitat

withinagriculturallandscapes.Inmanycountries,farmerscanreceivecost‐sharefunding

tocreatethesehabitats.Thesecost‐shareprogramscouldbeespeciallybeneficialfor

farmerswithpollinator‐dependentcrops,sincelocalhabitatcanprotectandenhance

nativebeesandthepollinationservicestheyprovide.Wisconsincranberrygrowersshould

beanespeciallylikelygrouptoparticipateinsuchprogramsduetotheirdemonstrated

commitmenttoenvironmentalstewardship,dependenceonpollinators,andavailabilityof

non‐croplandontheirfarms.Unfortunately,theiradoptionhasbeenverylow.Inorderto

increaseparticipation,wehavetounderstandwhygrowersarenotparticipating.

Therefore,theobjectiveofthisstudywastounderstandthebarriersthatpreventthe

implementationoffederallyfundedon‐farmconservationprogramsfornativebeeson

Wisconsincranberrymarshes.Wesentapapersurveyregardingfarmingpractices,

pollinators,conservation,anddemographicstothemailinglistoftheWisconsinState

CranberryGrowersAssociation(n=250).Wefoundthatwhileonly10%ofgrowerswere

awareofthefederalpollinatorcost‐shareprograms,onethirdofthemweremanaging

habitatforpollinatorswithoutfederalaidand50%wereinterestedinparticipatinginthe

program.Wealsofoundthat57%ofgrowersmanagehabitatforwildlife,althoughnone

receivecost‐sharefundingtodosoeither.Basedonresponsestoadditionalquestions,

participationincost‐shareprogramscouldbenefitfromoutreachactivitiesthatpromote

thecost‐shareprograms,areductionofbureaucratichurdlestoparticipate,andtechnical

supporttogrowersonhowtomanagehabitatforwildbees.

Keywords(4‐6):conservation,pollinator,agriculture,EQIP,classificationtreeanalysis

1.0Introduction

Theexpansionofmodernagriculturehasledtothedestructionandfragmentationof

habitat,resultinginamassivelossofbiodiversity(Bentonetal.2003,Foleyetal.2005).

Someofthisbiodiversityalsoprovidesvaluableecosystemservicestohumansandasthis

biodiversityislost,sotooaretheservicesitprovides.Insectsareonegroupoforganisms

thatarenegativelyaffectedbytheexpansionofagricultureandalsoprovidevaluable

servicestohumansincludingpestsuppressionandpollination(LoseyandVaughan2006,

Isaacsetal.2009).Byprovidinghabitatwithintheagriculturallandscape,someofthe

negativeeffectsofagricultureonbiodiversitymaybealleviated,allowingbeneficial

organismsandtheservicestheyprovidetopersist.

On‐farmconservationpracticestoestablishnon‐crophabitatwithinthefarming

landscaperepresentsoneapproachtolessenthenegativeeffectsofagriculturalexpansion.

Previousstudieshavedocumentedthevalueofsuchnon‐crophabitattobeneficialinsects

andtheservicestheyprovide(Merckxetal.2009,Scheperetal.2013,Morandinand

Kremen2013).BecauseofthelargeamountoftheEarth’slandareathatisusedfor

agriculture(Foleyetal.2011),incorporatingon‐farmconservationpracticeshasthe

potentialtomakeasubstantialcontributiontoprotectingbiodiversity.Becauseofthe

potentialvalueofon‐farmconservationtobiodiversity,manygovernmentsaroundthe

worldhavedevelopedconservationincentivesprogramstoencouragefarmerstomanage

non‐crophabitatinanefforttoprotectbiodiversity(Wadeetal.2008).Throughthese

programsfarmersreceivefinancialsupporttotakecroplandoutofproductionandinstead,

manageitforbiodiversitybyplantingnon‐crophabitat.

IntheUnitedStates,conservationincentivesprogramsexisttoencouragefarmersto

stopfarminghighlyerodibleland(e.g.,steephills),protectwaterwaysbyinstallingriparian

buffers,andmorerecently,providinghabitatforpollinators(VaughanandSkinner2008).

Farmerscanreceivecost‐sharefundingforpollinatorhabitatthroughanumberofdifferent

USDAconservationprogramssuchastheConservationReserveProgram(CRP)andthe

EnvironmentalQualityIncentivesProgram(EQIP)andpracticeswithinthoseprograms

(e.g.,fieldborders,conservationcover,hedgerows).Inaddition,asofthe2008USDAFarm

Bill,USDAconservationistsmustnowprioritizepollinatorsandpollinatorhabitatwhen

determiningpaymentsorreviewinganddevelopingconservationpractices(XercesSociety

2009).

Withtherecentdeclineinbothmanagedhoneybeesandwild,nativebees(Biesmeijer

etal.2006,Ellisetal.2010,Pottsetal.2010,Cameronetal.2011),theseprogramscouldbe

especiallybeneficialtofarmersgrowingpollinator‐dependentcrops,suchasWisconsin

cranberrygrowers.Cranberryisapollinator‐dependentcrop(DelaplaneandMayer2000)

forwhichgrowersspendthousandsofdollarseachyearonhoneybeehiverentals.

Additionally,Wisconsincranberrygrowersoftenownsignificantamountsofnon‐crop

supportlandthatcouldbeusedforpollinatorhabitat(ColquhounandJohnson2010).

Furthermore,theyhaveademonstratedappreciationforenvironmentalstewardshipwith

theirhighadoptionrateofintegratedpestmanagement(IPM)practices(DanMahr,pers.

comm.).Forexample,almostallofthesegrowershirecropscoutsinordertodetermine

whentosprayforpests,applyreducedriskpesticidesontheirmarshes,andusealternative

culturalpracticestocontrolpests(e.g.,flooding).Bycreatingpollinatorhabitatontheir

farms,cranberrygrowerscouldreceiveaneconomicallysignificantreturnontheirefforts

intheformofcroppollinationservicesprovidedbynativebees.

Despitethepossiblebenefitstogrowers,participationbyWisconsincranberry

growersinUSDAprogramstocreatepollinatorhabitatisnearlynon‐existent(JulieAmmel,

pers.comm.).Inordertoconvincegrowerstoparticipateintheseprograms,wehaveto

understandwhytheyaren’tcurrentlyparticipating.Somepossiblefactorsmayincludea

perceivedpestproblemfromconservationhabitat,lackofawarenessoftheprograms,lack

oftechnicalknowledgeorsupporttoimplementtheproject,oraperceptionthatthe

programsrequiretoomuchtime,space,ormoney.Byunderstandingwhygrowersarenot

participatingandwhichfactorsaremostimportantintheirdecisionmakingprocess,we

canmoreeffectivelyaddresstherootoftheproblem.

Inordertodeterminetheobstaclespreventinggrowersfromparticipatinginon‐

farmconservationprogramsfornativebeesandprovidepracticalsolutionsbasedon

growerinput,weconductedastate‐widegrowersurvey.Ourspecificobjectiveswereto

determinewhichfactorsaremostimportantinpredictingwhetherWisconsincranberry

growersare(1)activelymanagingtheirfarmstoencouragenativebeepollinators,(2)

activelymanaginghabitattoprotectotherwildlife,and(3)participatinginon‐farm

conservationincentiveprograms.Theresultsofthisstudywillinformtheoutreachand

educationeffortsofuniversityandagencypersonnelandidentifywaystoimprovefarmer

participationtosupportconservationpractices.

2.0 Methods

2.1Growersurvey

Wecreateda50‐questionwrittensurveyregardingcurrentfarmingpractices,

pollination,on‐farmconservation,anddemographics(Appendix4.1).Thesurveywas

reviewedbyseveralcranberrygrowers,conservationprofessionals,andextension

professorstoensureclarityandcompleteness.Questionswereadded,removed,oredited

basedonfeedbackfromthesegroups.ThesurveywasthensenttotheUniversityof

WisconsinSurveyCenterforreviewofquestionstructuretoensureinterpretability.The

finalsurveywasmailedtoeverycranberrygrowerontheWisconsinStateCranberry

GrowersAssociation(WSCGA)mailinglist(n=250)inJuneof2011.Duetoconfidentiality

policies,thelistwasnotsharedwiththeauthors,ratherthesurveysweredeliveredtothe

WSCGAofficeandtheofficestaffaddressedtheenvelopes.Acoverletterexplainingthe

purposeofthesurveyandastampedaddressedreturnenvelopewereincludedinthe

mailing.Areminderpost‐cardwassenttothesamerecipientsoneweekfollowingthe

initialmailing.

2.2Statisticalanalysis

Theresultsofthissurveyweresummarizedusingbothdescriptivestatisticsand

classificationandregressiontree(CART)analysis(R2.15.1,libraryrpart).Descriptive

statisticswereusedtodeterminethefrequencyofresponsestosurveyquestions.CART

analysiswasusedtodeterminewhichfactorsweremostimportantinpredictingthe

responseofgrowerstospecificquestionsregardingactivemanagementofhabitatforwild,

nativebees(Q22);alterationofmanagementtoprotectwild,nativebees(Q25);interestin

managingfornativebees(Q27);managementofhabitatforwildlife(Q29);andinterestin

participatinginaconservationincentivesprogramtocreatehabitatforwild,nativebees

(Q39).ACARTmodelisanon‐parametricmethodusedinordertodeterminewhich

factorsaremostimportantinpredictingvaluesofanotherfactor(De’athandFabricius

2000,ChangandWang2006).Forfactorswithdiscretevariable(e.g.,yes/noresponses)

theclassificationtreeisusedratherthanaregressiontree.Allothersurveyquestions

excepttheonedesignatedasthepredictedvariablewereincludedaspossiblepredictorsin

theCARTmodel.Theresultsofthisanalysishelpusidentifyfactorswhichclassifygrowers

intogroupswithsimilarresponsestoagivenquestion.Forexample,ifinterestlevelsin

conservationofwild,nativebeesisgroupedbycountybutparticipationislowinacounty

whereinterestishigh,extensionactivitiescanfocusonprovidinginformationand

technicalsupporttogrowersinthatcounty.Byunderstandingwhichfactorsbestpredict

currentmanagementorinterestbygrowers,futureextensionandoutreacheffortscanbe

bettertargetedtoaddressboththedesiredconservationoutcomesandthefactors

contributingtowhythegrowersdecidetoparticipateinon‐farmconservation.

3. Results

3.1 Responserateanddemographics

Theresponseratetooursurveywashigh(49%ofsurveysreturned,n=122).Survey

responsescamefromgrowersrepresentingabroadrangeofgeographiclocationsand

demographics.Growersrespondedfrom13countieswhichrepresentedboththecentral

andnortherngrowingregionsinthestate.Forty‐fourpercentofresponseswerefrom

WoodCountywhichhasthehighestdensityofcranberrygrowersinthestate.Theaverage

ageofrespondentswas45‐54yearsoldandtheaveragelengthoftimetheyhadbeen

growingcranberrieswas24.5years(±1.15SD,median23,range4‐77).Theaverage

propertysizewas1,115acres(±159SD,median450,range11‐11,000)includingon

average50‐149acresincranberryproduction.Inaddition,84%ofrespondentsindicated

thatgrowingcranberriesistheirprimarysourceofincome.

3.2 Activemanagementforbees

Despitealackofparticipationinpollinatorhabitatcost‐shareprogramsamong

cranberrygrowers(0%),33%ofgrowersactivelymanagehabitat(e.g.,plantflowering

shrubsandtrees,provideartificialnestboxes,providebrushpilesandmattressesfor

nesting)forwildbeeswithoutoutsideassistancefromaUSDAprogram.Additionally,30%

reportedthattheyhavealteredtheirmanagementinsomeotherway(e.g.,reduced‐risk

pesticides,timingofspray,delayedmowingofdikes)toencouragewildbeesontheir

property.Thethreefactorsthatweremostoftenselectedasveryorextremelyimportant

ingrowers’decisiontomanageforbeeswere(1)theimportanceofpollinationfor

cranberries,(2)environmentalstewardship,and(3)knowledgeaboutpollinatorhabitat

(fig.1).Ofthegrowerswhodonotmanageforbees,themostimportantfactorsinfluencing

theirdecisionwere(1)theimportanceofpollinationforcranberries,(2)theavailabilityof

technicalsupport,and(3)timecommitment.TheresultsofourCARTanalysisshowedthat

themostimportantpredictorofwhethergrowersmanagehabitatforbeeswaswhether

theyhadalsoalteredtheirmanagementinotherwaystoencouragewildbees(fig.2).Of

therespondentswhomanagehabitatforbees,56%ofthemhavealsoalteredtheir

managementinsomeotherway.Thenextbestpredictorvariablewaswhetherornotthe

growermanageshabitatforotherwildlife.Ofthosewhomanagehabitatforbees,51%also

managehabitatforwildlife.Regardlessofwhetherornotthegrowersmanageforwild

bees,87%respondedthatbeesareveryorextremelyimportanttocranberrypollination

and89%reportedthattheycurrentlyrenthoneybeesforpollination.

Thebestpredictorofwhethergrowersaltertheirmanagementinanywayother

thanhabitatmanagementtoprotectbees(e.g.,timingofspray,useofreducedtoxicity

pesticides)waswhethertheymanagehabitatforbees(fig.3).Thenextbestpredictorwas

howimportanttheyrated“environmentalstewardship”.Forty‐onepercentofgrowers

whoaltertheirmanagementforwildbeesratedenvironmentalstewardshipas

very/extremelyimportantintheirdecisiontomanageforbees.Theseresultsshowthat

growerswhomanagehabitatforwildlifeandvalueenvironmentalstewardshiparemore

likelytomanagehabitatforbeesoraltertheirmanagementinotherwaystoprotectbees.

3.3 Activemanagementofwildlifehabitat

Tounderstandfurtherhowgrowersperceiveon‐farmconservationingeneral,we

askedaseriesofquestionsregardingmanagementofhabitattoprotectwildlife.Wefound

that57%ofgrowersactivelymanagehabitatforthespecificgoalofprotectingwildlife,

althoughnonearereceivingcost‐sharefundingtodoso.Thefactorsthatweremostoften

selectedasveryorextremelyimportantininfluencingagrower’sdecisiontomanage

wildlifehabitatwere(1)knowledgeaboutwildlifehabitat,(2)knowledgeofwildlife,

environmentalstewardship,andrecreationsuchashuntingorhikingequallytiedfor

second,and(3)timecommitment(figure4).Ofthegrowerswhodonotmanagefor

wildlifehabitat,themostimportantfactorsintheirdecisionmakingwas(1)time

commitment,(2)financialcommitment,and(3)perceivedpestproblemsfromwildlife

habitat.TheCARTanalysisfurtherindicatedthatthemostimportantpredictorvariablefor

whetherornotgrowersmanagehabitattoprotectwildlifewashowimportanttheyrated

recreation(fig.5).Ofthosewhomanagehabitat,55%alsoratedrecreationas

very/extremelyimportant.Ofthosewhodidnotraterecreationasimportant,thenext

mostimportantpredictorvariablewasthenumberofyearsthegrowerhadbeengrowing

cranberries.Thirty‐twopercentofgrowerswhomanagehabitatforwildlifehavebeen

growingcranberriesformorethan28.5yearswhereasonly13%havebeengrowing

cranberriesforlessthan28.5years.

Theseresultssuggestthatgrowerswhomanageforwildlifehaveknowledgeofwildlife

andtheirhabitatrequirements,astrongenvironmentalstewardshipethicandinterestin

outdoorrecreationsuchashuntingorhiking.Whiletheyacknowledgethetime

commitmentasanimportantfactor,theotherfactorsoutweighthetimecommitment.

Theseresultsfurthersuggestthattheperceivedtimeandfinancialcommitment,inaddition

topossiblepestproblems,causesomegrowerstonotmanagewildlifehabitatontheir

farm.Growerswhovaluerecreationsuchashuntingorhikingaremostlikelytoalso

managewildlifehabitatbutofthosewhodon’tvaluerecreationashighly,thegrowerswho

havebeenfarmingforalongerperiodoftimearemorelikelytomanagewildlifehabitat.

3.4Participationinconservationincentivesprograms

Thirty‐onepercentofrespondentsindicatedthattheycurrentlyorhavepreviously

participatedinUSDA‐sponsoredconservationincentivesprogramsincludingEQIP(22%),

CRP(8%),theConservationReserveEnhancementProgram(CREP,2%),andtheWildlife

HabitatIncentivesProgram(WHIP,2%).Growerswere,however,splitonwhetherthey

wouldparticipateinconservationincentivesprogramsinthefuture,andmorewere

unlikelytoparticipateinaUSDA‐sponsoredprogram(36%)thananon‐USDA‐sponsored

program(26%).Wealsofoundthatthemostimportantfactorsdeterminingwhethera

growerparticipatedinaconservationincentivesprogramwere(1)theamountof

paperwork,(2)timecommitment,and(3)financialcommitment(figure6).Ofthegrowers

whodidnotparticipateinconservationincentiveprograms,themostimportantfactors

influencingtheirdecisionwere(1)amountofpaperwork,(2)timecommitmentand

environmentalstewardshipequally,and(3)awarenessoftheprograms.

Whilenoneoftherespondentsparticipateinanincentivesprogramforpollinator

habitat,andonly10%areawarethatsuchprogramsexist,50%ofgrowerswouldbe

interestedinparticipating.ACARTanalysisindicatedthatthemostimportantpredictor

variableforwhetherornotgrowersareinterestedinparticipatinginacost‐shareprogram

toinstallpollinatorhabitatontheirpropertywastheirinterestinmanaginghabitatfor

beesinthefuture(fig.7).Thenextbestpredictorvariablewaswhetherthegrower

respondedpositivelytotheusefulnessofaninformationalpamphletaboutUSDA

conservationincentivesprogramsforwildbees.Thefinalpredictorvariablewashow

importanttherespondentratedbeautyorlandscapingintheirdecisionprocess.Ofthe2%

ofrespondentswhoratedbeautyandlandscapingas“extremelyimportant”,nonewere

interestedinmanaginghabitatforbeesinthefuture,possiblybecauseofaperceptionthat

thishabitatwouldbeunattractive.

Theseresultssuggestthattheamountofpaperworkandtimecommitmentwere

enoughtodiscouragemanygrowersfromparticipatingintheprogramsdespitethe

importanceofenvironmentalstewardshiptothesegrowers.

3.5 Sourcesofmanagementinformationforgrowers

Inordertoaddressthefindingsabove,extensionandoutreacheffortsmustreach

thegrowers.Byunderstandingwhichsourcesofinformationgrowers’useorwanttouse,

extensioneffortscanbemoreeffectivebycommunicatingtogrowersthroughthese

channels.Currently,themostcommonsourcesofinformationarepapernewsletters

(90%),cropscouts(82%),andtheannualmeetingoftheWSCGA(CranberrySchool,81%).

Inthefuture,growersareinterestedinusingemaillistservs(38%)inadditiontopaper

newsletters(36%),andcropscouts(35%).Wealsocollectedinformationonsourcesthe

growersdonotwanttouseinthefuturewiththetopthreebeingsocialnetworkingsites

(85%),automatictextmessagealerts(61%),andemaillistservs(44%).Thisinformationis

alsousefulsothatextensionandoutreachisnotmisdirectedtothesesourcesto

disseminateinformation.

4.0Discussion

Despitetheirdemonstratedcommitmenttoenvironmentalstewardship,participation

inpollinatorhabitatcost‐shareprogramsbyWisconsincranberrygrowersisverylow.

ThroughawrittensurveyofWisconsincranberrygrowers,wefoundthatawarenessof

pollinatorhabitatincentivesprogramsisalsoverylow.Despitethelackofparticipationin

formalconservationprograms,athirdofgrowersarecurrentlymanaginghabitatfor

pollinatorsanyway.Thesesamegrowerswerealsomorelikelytomanagehabitatfor

wildlife.Growerswhowerenotmanaginghabitatforbeesorwildlifeweredeterredbya

lackoftechnicalsupport,andtheperceivedtimeandfinancialcommitments.Thissuggests

thatoutreachandextensioneffortsshouldfocusbothonpromotingpollinatorhabitat

incentivesprogramsaswellasprovidinginformationandtechnicalsupporttogrowers

interestedincreatingpollinatorhabitat.

Themoststrikingfindinginoursurveywasthat,despitealackofparticipationinthe

cost‐shareprogramsforpollinatorhabitat,athirdofWisconsincranberrygrowersare

managinghabitatforwildbeesanyway.Thesemanagementactivitiesincludeddelaying

mowingofnon‐cropareasuntilcranberrywasinbloom,plantingflowersandtreesthat

bloomthroughouttheseason,andprovidingnestinghabitatsuchasbrushpilesandbare

soil.Morethanhalfofthegrowerssurveyedalsomanagehabitatforwildlife,yetnone

receivedcost‐sharefundingtodoso.Thegrowerswhomanagedhabitatforwildlifewere

morelikelytovalueoutdoorrecreationsuchashuntingorhadbeengrowingcranberries

formanyyears.Wisconsincranberrygrowersappeartobemotivatedmorebytheir

commitmenttoenvironmentalstewardshiporanappreciationoftheoutdoorsthanby

financialincentivesdespitethecostofhabitatmanagement.Similartoourresults,Banack

andHvenegaard(2010)foundthatfarmerswhoparticipatedinbiodiversity‐friendly

farmingpracticesweremostcommonlymotivatedbyamoralobligationtocareforthe

environmentovereconomicfactors.Thegoalofon‐farmconservationistoprovidehabitat

inagriculturallandscapestoprotectandenhancebiodiversity.Whilefinancialincentives

programsareonewaytomotivategrowerstoprovidethishabitat,appealingtotheirsense

ofenvironmentalstewardshipmaybeanequallystrongandeffectivewaytoincreasethe

conservationofnon‐crophabitatonfarms.

TheminimalparticipationinconservationincentivesprogramsbyWisconsincranberry

growersseemstobeduemainlytoanaversiontobureaucratichurdlesandalackof

awarenessoftheprogramsratherthanlackofinterest.Lemkeetal.(2010)alsofoundthat

farmerswerediscouragedfromparticipatinginconservationpracticesontheirfarms

becauseofthecomplexityofpaperworkinvolved.InMichigan,whereadoptionofthe

pollinatorhabitatprogramshasbeenhigh,thekeytosuccesshasbeenactivepromotionof

theprograms(EricMader,pers.comm.)aswellasgoodfinancialincentivesofuptoa90%

cost‐share(FSA2010).Inotherregionsofthecountryandtheworld,successful

implementationofconservationprogramshasbeenaresultofengagedconservation

professionalsdevelopingpersonalrelationshipswiththefarmersandpromotingthe

benefitsofconservationthroughworkshopsandone‐on‐oneassistance(Mendhametal.

2007,Lemkeetal.2010,Whittenetal.2012).CurrentlyinWisconsin,minimaltechnical

supportisavailableforgrowersinterestedinparticipatinginon‐farmpollinator

conservationpractices,althoughinterestinpromotingtheseprogramsisgrowingatthe

statelevel(J.Ammel,pers.comm.).

Thisstudyhighlightsfourkeyareasthatcanbeaddressedtoincreaseparticipationin

cost‐shareprogramsaimedatcreatinghabitat.First,thespecificprogramsandpractices

intendedforpollinatorconservationneedtobepromotedinWisconsin.Onlyasmall

percentageofcranberrygrowerswereawareoftheprograms,althoughhalfofthegrowers

wereinterestedinparticipatinginacost‐shareprogramforpollinatorhabitat.Since80‐

90%ofthecranberrygrowersgettheirmanagementinformationfromindustry

newsletters,cropscouts,andCranberrySchool,thesewouldbeappropriateoutlets

throughwhichtopromoteconservationprograms.

Second,thepaperworkrequiredbythegrowerstoparticipateintheseprogramsneeds

tobereduced.Loweringthebureaucratichurdlestoparticipationwouldgreatlyreduce

thetimecommitmentandmakeparticipationeasier.InordertoparticipateinUSDA‐

sponsoredconservationincentivesprograms,growershavetogothroughalong,

bureaucraticprocessofdeterminingeligibilitythroughtheFarmServiceAgency(FSA),

developingconservationplans,selectingappropriateprogramsandpractices,and

submittingproposalstotheFSAthroughtheNRCS(USDA2013).Ontopofallofthe

paperworkalreadyrequiredbythegrowersregardingapplicationofpesticides,wateruse,

andpermitsformarshrenovationandexpansion,additionalpaperworkcandiscourage

growersfromparticipatingincost‐shareprograms(Lemkeetal.2010).Streamliningthe

processbyreducingtheamountofpaperworkcouldhaveabigimpactonparticipation.

Third,creatingpollinatorhabitatmayseemoverwhelmingbecauseoftheknowledge

requiredforestablishingandmaintainingnativeplants.Thereisaneedfortechnical

supporttodesignandimplementconservationplansthatincludepollinatorhabitat

(Traoréetal.1998,WhiteandSelfa2013),butwithoutapersonavailabletodirectthe

growers,answertheirquestions,andprovidepracticalon‐the‐groundsolutions,few

growerswillattempttoinstallpollinatorhabitat.Severalinformationalpamphletsandjob

sheetsexisttohelpgrowersplantheirpollinatorplanting(VaughanandMader2008,

VaughanandSkinner2008,Vaughanetal.2012),butwithmanyfarmerswithouthigh

speedinternet(VolenbergandJensen2010)accessingtheseresourcesisdifficult.

Andfinally,NRCSprogramadministratorsshouldestablishapeer‐mentoringprogram

toconnectgrowerswhoarecurrentlymanagingpollinatorhabitatwithgrowerswhoare

interestedinmanagingpollinatorhabitat.Sixty‐fourpercentofgrowersindicatedthatthey

getinformationregardingmanagementpracticesfromtheirneighborsandfriends,

suggestingthatpeermentoringcouldbeaneffectivewaytoincreaseparticipation.

Providinggrowerswithanexampleofanestablishedpollinatorhabitatplantingand

connectingthemwithagrowerwhohasgonethroughtheprocesshasthepotentialto

increasethesuccessofinterestedgrowerswhilereducingthedemandputonagency

personaltoaddresseveryconcernfromnewparticipants.Althoughitisbeyondthescope

ofthisresearchproject,furtherthoughtanddevelopmentwillneedtobegiventocreate

incentivesforgrowersactingasmentorstobepartoftheprogram.

Inordertomakeiteasierforgrowerstomanagehabitatforpollinatorsandparticipate

incost‐shareprogramstodoso,weneedtopromotetheavailableprograms,simplifythe

process,providedirection,andencouragepeermentorship.Thesestepshavethepotential

togreatlyincreaseparticipationamongWisconsincranberrygrowersaswellasother

pollinator‐dependentfruitcrops.Withoutthesesteps,theincentiveprogramsfor

pollinatorhabitatwilllikelycontinuestrugglingtogainparticipants.Byfollowingthesteps

outlinedabove,wecanmakeiteasierforfarmerstoparticipateandshowthaton‐farm

conservationisaprioritytotheUSDA.

Acknowledgements

Wethankallofthecranberrygrowerswhorespondedtooursurvey.Wealsothank

JulieDollandtheUniversityofWisconsinSurveyCenterforhelpwithsurveydevelopment,

JaneAndersonformailingthesurveys,TomEbert,JohnO’Day,JayneSojka,MaceVaughan,

andEricMaderforcommentingonearlydraftsofthesurvey,andDavidDuncanfor

assistantswiththestatistics.ThisresearchwasfundedbyaNorthCentralRegion

SustainableAgricultureResearchandEducation(SARE)GraduateStudentGranttoH.R.G.

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progressandprospects.PhilosophicalTransactionsoftheRoyalSocietyB‐BiologicalSciences363:831–847.

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aneraofclimatechangeandbiofuelsproduction.EnvironmentalManagement51:379–391.

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supportlandholderparticipation:Aframeworkandcasestudyassessment.EcosystemServices.

XercesSociety.2009.Invertebrateconservationfactsheet:2008FarmBill:Benefitstocrop

pollinators.

Figurecaptions

Figure1.Percentofgrowersresponding“very”or“extremely”tohowimportanteach

factorisintheirdecisionwhetherornottomanageforwild,nativebees(Q26).

Figure2.Aclassificationtreethatpredictswhethergrowersrespondedpositivelyto

managinghabitatforwildbeesontheirfarm.Cranberrygrowerswhomanagehabitatfor

beesarealsolikelytohavealteredtheirmanagementinsomeotherwaytoprotectbees

andmanagehabitatforwildlife.56%ofgrowerswhomanagehabitatforwildbeeshave

alsoalteredtheirmanagementinsomeotherwaytoprotectbeesasopposedto21%who

havenotalteredtheirmanagementpractices.51%ofgrowerswhomanagehabitatfor

wildbeesalsomanagehabitatforwildlifeasopposedto5%whodonot.

alteringtheirmanagementinsomewaytoprotectwildbeesontheirfarm.59%ofgrowers

whohavealteredtheirmanagementinsomewaytoprotectbeesalsomanagehabitatfor

wildbeesasopposedto41%whodonot.41%ofgrowerswhohavealteredtheir

managementtoprotectbeesalsomanagehabitatforwildlifeasopposedto19%whodo

factorisintheirdecisionwhetherornottomanagehabitatforwildlife(Q32).

managinghabitatforwildlife.55%ofgrowerswhomanagehabitatforwildliferated

recreationsuchashuntingorhikingasveryorextremelyimportantintheirdecisionto

managehabitatforwildlife.45%ofgrowerswhomanagehabitatforwildliferated

recreationasonlyslightlyornotatallimportantintheirdecisiontomanagehabitatfor

wildlife.32%ofgrowerswhomanagehabitatforwildlifeanddidnotconsiderrecreation

asveryimportanthadbeengrowingcranberriesformorethan28.5years.Only13%of

growerswhomanagehabitatforwildlifeanddidnotraterecreationasimportanthave

beengrowincranberriesforlessthan28.5years.

factorisintheirdecisionwhetherornottoparticipateinaconservationincentives

program(Q38).

Figure7.Aclassificationtreethatpredictswhethergrowersareinterestedinparticipating

inacost‐shareprogramforwildbeesinthefuture.98%ofgrowerswhoareinterestedin

thecost‐shareprogramwerealsointerestedinmanaginghabitatforbeesinthefuture.

95%ofgrowerswhowereinterestedinabeehabitatcost‐shareprogramexpressedutility

inaninformationalpamphletaboutUSDAcost‐shareprogramsforwildbees.And95%of

growerswhowereinterestedincost‐shareprogramsforpollinatorsratedbeautyand

landscapingaslessthanextremelyimportantintheirdecisiontomanagehabitatforbees.

Financial commitment

Time commitment

Space requirements

Availability of cost share programs

Availability of techincal support

Environmental stewardship

Encouragement of neighbor or friend

Knowledge about wild bees

Knowledge about pollinator habitat

Perceived weed problems from pollinator habitat

Perceived pest problems from pollinator habitat

Beauty or landscaping

0 10 20 30 40 50 60 70 80 90

Importance of pollination for cranberries

Farmers who currently manage habitat for wild beesFarmers who do NOT manage habitat for wild bees

Percent responding very/extremely important

Figure 1110

Growers who actively manage habitat to encourage wild bees on their property (Q22)

YES(56%)

NO(21%)

Altered management for wild bees (e.g., spray at night)

Manages habitat for wildlife

YES(51%)

NO(5%)

Figure 2111

Growers who have altered their management in some way to protect wild bees (Q25)

YES(59%)

NO(41%)

Manage habitat for bees

Manages habitat for wildlife

YES(41%)

NO(19%)

Figure 3112

Time commitment

Space requirements

Knowledge of wildlife

Knowledge about wildlife habitat

Perceived weed problems from wildlife habitat

Perceived pest problems from wildlife habitat

Beauty or landscaping

Recreation, such as hunting or hiking

0 10 20 30 40 50 60

Farmers who manage habitat for wildlifeFarmers who do NOT manage habitat for wildlife

Figure 4113

Growers who manage habitat for wildlife (Q29)

Very/extremely(55%)

Not/slightly(45%)

How important the grower rates recreation such as hunting or hiking in their decision to manage habitat for wildlife

Years growing cranberry

>28.5 years(32%)

<28.5 years(13%)

Figure 5114

0 10 20 30 40 50 60

Time commitment

Awareness of programs

General interest

Amount of paperwork

Government sponsorship of the program

Farmers who have participated in USDA conservation incentives programsFarmers who have NOT participated in USDA conservation incentives programs

Figure 6115

Growers who expressed interest in participating in a cost-share program for pollinators

YES(98%)

NO(1%)

Interested in managing habitat for wild bees in the future

Informational pamphlet about USDA cost-sharing programs for wild bees would be useful

YES(95%)

NO(3%)

Not extremely(95%)

Extremely(0%)

Importance of beauty or landscaping in their decision to manage habitat for wild bees

Figure 7116

Cranberry Grower Survey

1. Are you currently acting as the primary farm operator for your cranberry farm? Acting as the primary farm operator would include handling day to day operations and making decisions regarding farming practices for cranberry production done on your farm.

Yes Go to question 2

We would appreciate your assistance in passing this survey on to the person who is the primary farm operator for your Cranberry farm.

If you are unable to pass the survey on to that person, please make note of that here and return the blank survey in the enclosed postage paid envelope.

Thank you!

This study is being conducted in order to understand how cranberry growers regard on-farm conservation programs in general and pollinator conservation programs in particular.

Your answers will be kept confidential, and not released in a way that would allow you to be identified.

2. Within the past 5 years, if you ever irrigated, in general, what time of day did you irrigate your cranberry beds? (Check all that apply)

Between 3:00 p.m. and 7:00 p.m.

Between 8:00 a.m. and 3:00 p.m.

Before 8:00 a.m.

After 7:00 p.m.

I never irrigated over the past 5 years

Before 8:00 a.m.

Between 8:00 a.m. and 3:00

Between 3:00 p.m. and 7:00

p.m.After 7:00

I did not apply in past 5 years

a. Insecticide

3. Within the past 5 years, if you applied any of the following substances, what time of day did you usually apply them to your cranberry beds? (Check all that apply)

b. Herbicide

c. Fungicide

4. Within the past 5 years, if you applied any of the following substances, how many applications, on average, did you spray per year of each of the following? If you did not spray at all, please write ‘0’ for that substance.

a. Insecticide

b. Herbicide

c. Fungicide

d. Other, please describe

Number of applications

per year

MANAGEMENT OF CRANBERRY MARSHES

This section is about current management practices and where you obtain information on management practices.

5. Within the past 5 years, did you ever use the following types of insecticide products on your cranberry beds?

a. Insect growth regulators such as Confirm or Intrepid

b. Neonicotinoids such as Assail

c. Organophosphates such as Diazinon or Lorsban

d. Some other products, please describe

Yes No

6. Is your farm certified organic?

7. Do you hire a scout to monitor for insect pests?

8. Within the past 5 years, which of the following methods did you use to determine when to spray for insect pests? Did you use…

a. ...a calendar schedule?

b. ...scout reports?

c. ...some other method? please describe

Yes No

9. Within the past 5 years, what insect pest management strategies did you use in addition to or instead of insecticides? Did you use…

a. ...flooding?

b. ...biological control?

c. ...sanding?

d. ...some other strategy? please describe

Yes No

10. Below is a list of sources of information about pest, nutrient, water, frost and other management practices. For each source of information, please indicate if you have used that source in the past, if you are using it now, if you want to use it in the future, or if you have NEVER used that source of information, and would not want to in the future. (Check all that apply)

c. Natural Resources Conservation Service (NRCS) Staff

Used it in the past

Use it now

Want to use it in the future

Never used it and will not in the

futurea. Crop Scout

b. University Extension Agent

d. Neighbor or friend

e. Cranberry School

f. Information hotline (phone)

g. Newsletter (paper)

h. Email listserv

i. Text message (automatic alerts)

j. Social networking site (Facebook, Twitter)

13. Have you ever rented honey bees for pollination in the past?

12. How many hives per acre?

11. Do you currently rent honey bees for pollination?

Go to question 13

k. Website (please list below)

l. Other (please list below)

This section is about your current pollination practices and your awareness about wild bees and pollinator habitat.

POLLINATORS - WILD AND MANAGED

15. How many hives per acre?

14. Do you use commercial bumble bees for pollination?

Go to question 16

16. Have you noticed a change in the availability of honey bee hives in the past 5 years?

Yes Please explain

17. Have you observed a change in the quality of rented honey bee hives in the past 5 years?

Yes Please explain

18. How familiar are you with Colony Collapse Disorder (CCD)?

Somewhat familiar

Slightly familliar

Not at all familiar

Very familiar

Extremely familiar

19. Can you distinguish between wild bees and honey bees?

20. How important do you think honey bees are for cranberry pollination?

Somewhat important

Slightly important

Not at all important

Very important

Extremely important

21. Are you aware of any wild bees on your property?

22. Do you actively manage habitat to encourage wild bees on your property?

Yes Please explain

23. If you do manage habitat for wild bees, did you receive cost-share funding to do this?

Yes Through whom?

24. Are you aware of cost-share programs for establishing pollinator habitat?

25. Have you altered your management in any way to encourage wild bees on your property?

Yes Please explain

Not at all Slightly Somewhat Very Extremelya. Financial commitment

Not applicable

b. Time commitment

c. Space requirements

d. Availability of cost share programs

26. How important are each of the following in your decision about whether or not to manage for wild bees?

e. Availability of technical support

f. Environmental stewardship

g. Encouragement of neighbor or friendh. Knowledge about wild bees

i. Knowledge about pollinator habitat

j. Perceived weed problems from pollinator habitat

k. Perceived pest problems from pollinator habitat

l. Beauty or landscaping

m. Importance of pollination for cranberries

n. Other (please explain)

Go to question 24

27. If you do not currently manage for wild bees on your property would you be interested in managing for wild bees in the future?

28. Which of the following would be useful to you?

UsefulNot

usefula. Field day demonstration of a pollinator habitat project

b. Informational pamphlet about wild bees

c. Field guide to wild bees

d. Informational pamphlet about USDA cost-sharing programs for wild bees

e. Website about wild bees

f. Website about pollinator habitat

g. Website about USDA cost-sharing programs for wild bees

h. Other (please explain)

29. Do you currently manage habitat (prairie plantings, woodlots, wetland, etc.) for the specific goal of protecting wildlife (birds, beneficial insects, mammals, etc.)?

Go to question 32

30. If yes, do you receive cost-share funding to support these conservation management activities?

31. Through whom do you receive cost-share funding to support these conservation management activities?

The next questions are about on-farm conservation programs in general.

Go to question 32

ON-FARM CONSERVATION PROGRAMS

32. How important are the following in your decision whether or not to manage habitat for wildlife such as birds, beneficial insects, and mammals?

a. Financial commitment

b. Time commitment

c. Space requirements

d. Availability of cost share programs

e. Availability of technical support

f. Environmental stewardship

g. Encouragement of neighbor or friendh. Knowledge of wildlife

i. Knowledge of wildlife habitat

j. Perceived weed problems from wildlife habitat

k. Perceived pest problems from wildlife habitat

l. Beauty or landscaping

m. Recreation, such as hunting or hiking

Not at all Slightly Somewhat Very ExtremelyNot

applicable

n. Other (please explain)

33. Do you or have you ever participated in any of the following United States Department of Agriculture (USDA)-sponsored conservation incentive programs? (Check all that apply.)

Environmental Quality Incentives Program (EQIP)

Conservation Reserve Enhancement Program (CREP)

Conservation Reserve Program (CRP)

Wildlife Habitat Incentives Program (WHIP)

Other, please explain

34. Do you currently participate in the Whole Farm Planning Incentives Program (WFPIP)?

35. Do you currently participate in any programs that address the following environmental/conservation issues? (Check all that apply.)

Water quality and conservation

Pest management

Nutrient management

Soil conservation

36. In the future, how likely are you to participate in a USDA-sponsored conservation incentive program?

Somewhat unlikely

Very unlikely

Extremely unlikely

Not sure

Somewhat likely

Very likely

Extremely likely

37. In the future, how likely are you to participate in a non-USDA-sponsored conservation incentive program?

Somewhat unlikely

Very unlikely

Extremely unlikely

Not sure

Somewhat likely

Very likely

Extremely likely

Very ExtremelyNot

applicable

38. How important are the following in your decision whether or not to participate in a conservation incentive program?

a. Financial commitment

b. Time commitment

c. Availability of cost share programs

d. Availability of technical support

e. Environmental stewardship

f. Encouragement of neighbor or friend

g. Awareness of programs

h. General interest

i. Amount of paperwork

Not at all Slightly Somewhat

k. Other (please explain)

j. Government sponsorship of program

39. Would you be interested in participating in a cost-share conservation program to enhance wild bees through the planting of pollinator habitat on your property?

40. Do you know who your NRCS officer or representative is?

41. Are you comfortable working with or getting information from your NRCS officer or representative?

42. What is your age?

Less than 25 years old

65 or older

43. What is your gender?

Female

44. In which county (or counties) do you grow cranberries?

45. How many acres of cranberries do you manage?

150 – 300 acres

50 – 149 acres

Less than 50 acres

Over 300 acres

46. How many total acres do you own or manage, including all cranberry and non-cranberry?

47. How long have YOU been growing cranberries?

These last questions are about you.

YOUR BACKGROUND 127

50. Is growing cranberries your primary source of income?

THANK YOU for your participation!

If you have any questions or concerns, please contact Hannah Gaines by phone (774-392-0498) or email (hgaines@gmail.com).

If there is anything else you would like us to know, please use the space below to do so.

48. How long has YOUR FAMILY been growing cranberries?

49. Do you regularly attend Cranberry School?

THESISCONCLUSION

Theresearchpresentedinmydissertationcontributestoourunderstandingofhow

localandlandscapefactorsinfluencebeesandcranberrypollination.Fromthescaleofa

singlecranberryflowertothelandscapeofcentralWisconsin,theresultsofmy

dissertationprovidenewevidenceregardingthepollinationrequirementsofcranberry,the

contributionofnativeandmanagedbeestocranberryyield,andtheinteractingeffectof

landscapeonhivestockingdensities.Thisresearchalsoprovidespracticalinformation

thatcanbeappliedtofuturemanagementandconservationpractices.

1. NativebeesintheWisconsincranberryagroecosystemrespondpositivelytoa

gradientofincreasingwoodlandinthesurroundinglandscape.Similartothe

findingsofpreviousresearchinotheragroecosystems,Ifoundthatnativebee

abundanceandspeciesrichnessincreaseastheamountofwoodedhabitatinthe

surroundinglandscapeincreases.Sinceagriculturallandscapesarehighlymanaged

andprovideforagingresourcesforonlyashorttimeduringthegrowingseason,close

proximitytonon‐crophabitatswouldallowbeestouseresourcesinboththecropand

non‐crophabitats.

2. Thecontributionofnativebeestocranberryyieldishighlyvariablefromyearto

yearandonlybecomesevidentwithyearsofdatafrommanysites.WhileIwas

unabletofindevidenceofaneffectofnativebeestocranberryyieldinmyfieldstudies

(chp.3),whenIanalyzedoveradecadeworthofhistoricaldatafromthegrowers,I

foundevidencethat,intheabsenceofhoneybees,cranberrymarshesinhighwooded

landscapesachievedamarginallyhigheryieldthanmarshesinlowwoodland

landscapes(chp.2).Sincenativebeeabundanceandspeciesrichnessincreasedwith

theamountofwoodlandinthesurroundinglandscape,itseemslogicalthatthis

marginalincreasemaybeduetopollinationbynativebees.Additionally,studiesfrom

othersystemshavefoundthatcropyieldincreaseswithbeediversity,further

supportingthehypothesisthattheyieldincreaseisduetonativebees.Inashortterm

fieldstudy,anyeffectofnativebeesonyieldislikelymaskedbythestronginfluenceof

localmanagementpracticesincludingtheuseofmanagedhoneybees.Myresults

suggestthattheuseoflargehistoricaldatasetscouldbeavaluablesourceof

informationregardingthecontributionofnativebeestocropyieldforadiversityof

croppingsystemsaroundtheworld.Furthermore,thisdatashouldbeavailablefor

manycropsasgrowersoftenkeepcarefulrecordsoftheiryieldandmanagement

practices.

3. Non‐bioticfactorscontributesignificantlytocranberrypollination.Theresultsof

myfieldandgreenhouseexperimentsclearlydemonstratethat,contrarytoprevious

research,intheabsenceofbees,cranberryisstillabletoproduceviablefruit(chp.1).

Atthesametime,mydataalsosupportpreviousresearchconfirmingthatcranberryis

unlikelytoself‐pollinate.Previousstudiesweredesignedtocompareself‐pollination

andbioticpollinationonly,ignoringthepossibilityofalternativemechanisms.Isuggest

thatpollinationwithoutbeesisduetothephysicalagitationoftheplants(e.g.,bywind)

causingflowerstobumpintoeachother,resultinginthetransferofpollenbetween

flowers.Thismechanismisfacilitatedbyhorticulturalpracticesincommercial

cranberryproductionwhereplantsgrowdenselyandproduceasuperfluousnumberof

flowers.Muchofthecranberrypollinationliteraturewasdonedecadesagowhen

yieldsweremuchlower.Advancesintechnologyandmanagementpracticeshaveledto

higheryieldsandmoredenselyplantedcranberryuprights,suggestingthat

horticulturaldifferencesmaybepartiallyresponsiblefordifferencesbetweenmy

resultsandolderstudies.Innaturalbogcommunities,wherecranberrygrowssparsely,

thesefindingsmaynotbeapplicable.

4. Theeffectivenessofhoneybeesascranberrypollinatorsislandscapedependent.

Inlowwoodlandlandscapes,yieldisstronglycorrelatedwithhivedensity,butinhigh

woodlandlandscapes,thereisnoevidencethatincreasinghivedensityhasanyeffecton

yield(chp.2).Thissuggeststhatonsomemarshes,bringinginhoneybeesfor

pollinationhasabigeffect,whileonothers,honeybeesprovidelittleornoadded

benefit.Oneexplanationforthispatternisthathoneybeesmaybedrawnawayfrom

themarshestoforageonnon‐cropfloralresources.Apreviousstudyincranberry

foundthathoneybeesreturningtothehivecarriedverylittlecranberrypollen,

supportingtheideathatthebeesareforagingelsewhere.Thishasimplicationsfor

managementdecisionsincludingwhethertousehoneybeesforpollinationand

whetherprovidingsupplementalforagingresourceswithinagriculturalareasmay

enhancethecroppollinationactivityofhoneybees.

5. Cranberryyieldrespondsmoststronglytolocalfactorsincludinghoneybeehive

stockingdensityandfloweringuprightdensity.Thissuggeststhatgrowershave

quiteabitofcontroloveryieldthroughtheirmanagementdecisions.Therewasalsoan

interactingeffectoffloraldensityandhivestockingdensity(chp.3)indicatingthatif

growerscanincreasetheirfloraldensity,theywillalsobeincreasingtheamountof

pollinationservicescontributedbybees.Alternatively,iffloraldensityislow,

increasingthenumberofbeeswillnotleadtoahigheryield.

6. Interestamongcranberrygrowersregardingon‐farmpollinatorhabitat

conservationishigh,butalackoftechnicalsupportandbureaucratichurdles

createbarrierstotheirparticipationinfederalcost‐shareprograms.Theresults

ofmyresearchsuggestthatparticipationcouldbeincreasedthroughoutreachactivities

thatpromotethecost‐shareprograms,areductionofbureaucratichurdlesto

participate,andincreasingtheavailabilityoftechnicalsupporttogrowersonhowto

managehabitatfornativebees(chp.4).Ialsosuggestthatapeer‐mentorprogrammay

beusefulasmanyofthegrowersreportedgettingmanagementinformationfromtheir

friendsandneighbors.

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