Identifying native plants for coordinated habitat ...€¦ · Natural and semi-natural habitats in...

J Appl Ecol 20181ndash12 wileyonlinelibrarycomjournaljpe emsp|emsp1copy 2018 The Authors Journal of Applied Ecology copy 2018 British Ecological Society

Received7June2018emsp |emsp Accepted12October2018DOI1011111365-266413304

R E S E A R C H A R T I C L E

Identifying native plants for coordinated habitat management of arthropod pollinators herbivores and natural enemies

Ola Lundin12 emsp|emspKimiora L Ward1emsp|emspNeal M Williams1

1DepartmentofEntomologyandNematologyUniversityofCaliforniaDavisDavisCalifornia2DepartmentofEcologySwedishUniversityofAgriculturalSciencesUppsalaSweden

CorrespondenceOlaLundinEmailolalundinsluse

Funding informationUSDANaturalResourcesConservationServiceGrantAwardNumber68-9104-5-343USDAAgriculturalMarketingServiceGrantAwardNumber16-SCBGP-CA-0035CarlTryggersStiftelsefoumlrVetenskapligForskningUSDANationalInstituteofFoodandAgricultureGrantAwardNumber2012-51181-20105-RC1020391

HandlingEditorJacquelineBeggs

Abstract1 Providingnoncrop flowering resources inagricultural landscapes iswidelypro-motedasastrategytosupportarthropodsthatdeliverpollinationandpestcon-trol services However management options have largely been developedseparatelyforpollinatorsandnaturalenemieswhereaspossibleeffectsoninsectherbivoressuchascroppestshaveoftenbeenoverlookedAfirstcriticalstepfordesignand implementationofmultifunctionalplantingsthatpromotebeneficialarthropodswhilecontrolling insectpests is to identifysuitableplantspeciestouse

2 WeaimedtoidentifyCalifornianativeplantsandmoregenerallyplanttraitssuit-ableforthecoordinatedmanagementofpollinators (wildbeesandhoneybees)insectherbivoresandarthropodnaturalenemies(predatorsandparasiticwasps)Weestablished43plantspecies inacommongardenexperimentandsampledarthropodsbyweeklynetting (wildbees)observations (honeybees)orvacuumsampling (insect herbivores arthropod predators and parasitic wasps) duringpeakbloomofeachplantspeciesover2years

3 PlantspeciesdifferedinattractivenessforeacharthropodfunctionalgroupFloralareaofthefocalplantspeciespositivelyaffectedhoneybeepredatorandpara-siticwaspattractivenessLaterbloomperiodwasassociatedwithlowernumbersofparasiticwaspsFlowertype(actinomorphiccompositeorzygomorphic)pre-dictedattractiveness forhoneybeeswhichpreferredactinomorphicovercom-positeflowersandforparasiticwaspswhichpreferredcompositeflowersoveractinomorphicflowers

4 Acrossplant species herbivore predator andparasiticwasp abundanceswerepositivelycorrelatedandhoneybeeabundancecorrelatednegativelytoherbivoreabundance

5 Synthesis and applicationsWeusedatafromourcommongardenexperimenttoinformevidence-basedselectionofplantsthatsupportpollinatorsandnaturalen-emieswithoutenhancingpotentialpestsWerecommendselectingplantspecieswithahighfloralareapergroundareaunitasthismetricpredictstheabundancesofseveralgroupsofbeneficialarthropodsMultiplecorrelationsbetweenfunc-tionallyimportantarthropodgroupsacrossplantspeciesstresstheimportanceofamultifunctionalapproachtoarthropodhabitatmanagement

2emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL

1emsp |emspINTRODUC TION

Integration of functionally important biodiversity and associatedecosystemservicesintocropproductionisimportantforthelong-term sustainability of agricultural systems (Cardinale etal 2012Kremen amp Miles 2012) Crop pollinators and natural enemies tocroppestsaretwoprimaryexamplesofsuchfunctionalbiodiversitythathave receivedparticularattention (Kleinetal2007LoseyampVaughan2006)Increaseduseofthesesupportingecosystemser-viceshasthepotentialtoreduceanthropogenicinputstoagriculturesuch as pesticides and intensive honeybee keeping practices andtherebycontributetosustainableagriculture (BommarcoKleijnampPotts 2013)Despite great potential the ability to integrate sup-portingecosystemservices intocropproduction isconstrainedbylimitedguidanceonhowthiscanbeachievedinpracticeThechal-lengeismagnifiedwhenmultipleservicesaresoughtsimultaneouslyaspotentialtrade-offsmarginalgainsandlossesmustbeconsidered(BennettPetersonampGordon2009TamburiniDeSimoneSiguraBoscuttiampMarini2016)

Croppollinationandpestcontrolaremobile-agent-basedecosys-temservices(Kremenetal2007)andinthecaseofpestdamagemdashdisservices (Zhang Ricketts Kremen Carney amp Swinton 2007)andas such theorganisms responsible fordelivering themcanbeaffectedbysimilarenvironmentaldrivers(Shackelfordetal2013)Naturalandsemi-naturalhabitats intheagricultural landscapeforexamplepromotebothpollinators(Rickettsetal2008)andnaturalenemiestocroppests(Chaplin-KramerOrsquoRourkeBlitzerampKremen2011)Managingforcroppollinationandpestcontrolprovidedbyarthropods in agriculture often entails actions that provide foodnesting or overwintering habitat and protection from agriculturaldisturbancefor thetargetserviceproviders (Garibaldietal2014LandisWratten ampGurr 2000)Management actions to promotepollinatorsandnaturalenemieshavehoweverlargelybeendevel-opedseparatelyandthepossibleeffectsoninsectherbivoressuchascroppestshaveoftenbeenoverlookedHabitatswithfloweringresources forexamplearetypicallyestablishedeitherforpollina-torsor fornaturalenemiesalthougheachof theseplanting typesmayaffectbothorganismgroups(FiedlerLandisampWratten2008WrattenGillespieDecourtyeMaderampDesneux2012)Therehasbeen limited effort to integrate provision of flowering resourcesforpollinationandpestcontrol(butseeGrabPovedaDanforthampLoeb2018SutterAlbrechtampJeanneret2018)Thisissurprisinggiventhatforgrowersitisimportantthatplantingsforpollinatorsdonotincreasepestpressureanddesirablethattheyprovidebiologicalpestcontrolservices(SidhuampJoshi2016)Consideringpollinationandpestcontrolservicesintandemalsohasgreatpotentialtomakehabitatplantingsmorecosteffectiveandincreasethelikelihoodof

adoption(GarbachampLong2017MorandinLongampKremen2016)Afirstcriticalsteptowardsdesignandimplementationofmultifunc-tionalplantingsisidentificationofsuitableplantspeciestousethatsupportpollinatorsandnaturalenemiesbutnotpests

Nativeplantsinparticularshowpromiseforuseinhabitatman-agement for pollinators and natural enemies as they are adaptedforgrowingunderlocalconditionsandarelesslikelytobeinvasive(FiedlerampLandis2007a IsaacsTuell FiedlerGardinerampLandis2009)Useofnativeplantshoweveralsocomplicatesplantchoicebecauseplantspeciesthataresuitableforpropagationandattrac-tiveforarthropodsneedtobeidentifiedinaregion-specificmannerTheprocessofselectingplantspeciesformultifunctionality isfur-thercomplicatedbecausethebestspeciesforsupportingpollinatorsmay ormay not support natural enemies and vice versa and fur-thermoretrade-offsbetweenbenefitingbeneficialarthropodsandpromotingpestsmustbeconsideredThisselectionprocesswouldbegreatlyfacilitatedifkeyplanttraitscouldbe identifiedthatareassociatedwithpollinatorherbivoreandnaturalenemyattractive-nessStudiesofplantsnativetoMichigan(US)showedthatthetim-ingofpeakbloomandfloralareawerepositivelyrelatedtonaturalenemyabundance (FiedlerampLandis2007a2007b)Bloomperiodand floral areawere also positively related to the abundance anddiversityofwildbeesvisitingplantswhereasfloralareawasunre-latedtotheabundanceofhoneybees(TuellFiedlerLandisampIsaacs2008)Apartfrombloomperiodandfloralareatheaccessibilityofresources(nectarandpollen)toarthropodsisalsolikelytoinfluenceattractivenessResourceaccessibilityisdrivenbyseveralinteractingfactorsincludingcorollawidthanddepthwhetherresourcesareof-feredinlargevsmanysmallflowers(egcompositeinflorescencesinAsteraceae)andarthropodbodyandmouthpartsize(Carvalheiroetal2014vanRijnampWaumlckers2016Waumlckers2004)Suchmul-tivariate interaction complicates selection of a single informativeflowertraitIthasnotbeentestedwhetherflowertype(actinomor-phic compositeor zygomorphic flowers) couldserveasageneralproxy for a set of interacting factors affecting arthropod attrac-tiveness Actinomorphic and composite flowers generally presentmoreaccessibleresourceswithlessandmoresplittingofresourcesbetweenflowersrespectivelywhilezygomorphicflowersgenerallyhave less accessible resources due to deeper corollas or specificflowerhandlingrequiredtoaccessresources

The overall aim of our studywas to identify California nativeplantsandmoregenerallyplanttraitssuitableforcoordinatedhab-itatmanagement of arthropodpollinators herbivores andnaturalenemiesandpromoteintegratedecosystemservicesinagriculturallandscapesMorespecificallyweask(a)whichnativeplantsamongourcandidatesetattractthehighestabundancesofwildbeeshon-eybees herbivores predators and parasiticwasps (b) if the total

K E Y W O R D S

biologicalcontrolhoneybeemultifunctionalitynativebeenaturalenemyparasiticwasppollinatorwildbee

emspensp emsp | emsp3Journal of Applied EcologyLUNDIN et aL

abundances of arthropods within these functional groups acrossplantspeciesarerelatedtothepeakfloweringweekfloralareaorflowertypeofthefocalplantspeciesand(c)ifthetotalabundancesofarthropodswithinthesefunctionalgroupsarecorrelatedtoeachotheracrossplantspeciesIngeneralweexpectedhigherarthropodnumbersonplant specieswithhigh floral areaandactinomorphicflowertypeduetoeasyaccesstolargeresourceamountsandthatarthropod numberswould be higher on plantswith a later bloomperioddue tobuildupofarthropodpopulationsizesover thesea-sonWealsoexpectedthattheabundancesofseveralgroupsofar-thropodswouldbepositivelycorrelatedacrossplantspeciesduetosharedresponsestoplanttraits

2emsp |emspMATERIAL S AND METHODS

21emsp|emspSelection of plants

Wetestedatotalof43plantspecies(Table1)Selectedspecieswereforbs thatwere drought-tolerant native to California (one excep-tion is listed below) and as a group covered a range of floweringperiods throughout the seasonA further consideration for selec-tion of most plant species was indications that they could be at-tractive tobeesbasedonbeing listedasnectar andpollenplantsfor honeybees (Vansell 1941) being recommended as pollinatorplants (XercesSociety2018)being listedasassociatedwithbeesinCalflora(2017)orbasedonearliercollecteddataonbeeattrac-tiveness(Williamsetal2015)Withtheexceptionofoneselectedplant speciesAntirrhinum cornutum forwhichseedwashandcol-lected a further criterion that restricted selectionwas that plantmaterialneededforpropagationwascommerciallyavailableeitherasseedsorplugplantsWealsoincludedAchillea millefoliumandtheshrubEriogonum fasciculatumbasedonfindingsthattheseplantsareattractive for locally abundant natural enemies (Morandin LongPease amp Kremen 2011 Pisani-Gareau Letourneau amp Shennan2013)FinallyweincludedFagopyrum esculentumwhichisanexoticspeciesknowntobeattractivefornaturalenemiesandwidelyusedinconservationbiologicalcontrol(Fiedleretal2008)NoselectedplantsweremajorweedsofcropsorpasturesHoweverAmsinckia intermedia and Calandrinia menziesiicanalthoughtheyaredesirablecomponentsofwildlandsbecomeminorweedsincertainsituations(UCIPM2018)

22emsp|emspStudy site and design

We collected data over two consecutive seasons 2015-2016 attheHarryHLaidlawJrHoneyBeeResearchFacility(38deg32prime11PrimeN121deg47prime18PrimeW)atUniversityofCaliforniaDavisCAUSADavishasaMediterraneanclimatewithdryhotsummersandcoolrainywin-tersSoiltypeonthesiteisaYolosiltloam(USDANRCS2017)Landusewithin1kmofthestudysiteisdominatedbyagriculturallandswitharangeoffieldandorchardcropsinsmallfieldsTwentytofortyhoneybeeApis mellifera Lcolonieswerekeptatthesitewithin100mfromourexperimentInadditioneightmanagedresearchcolonies

of theyellow-facedbumblebeeBombus vosnesenskiiRadoszkowskiwereonsite in2015andthusbothwildandmanaged individualsofthisspeciesareincludedamongthegrouphenceforthreferredtoaswildbeesinouranalysesThestudyusedarandomizedcompleteblock design with each plant species growing in a monospecificoneby1mplotineachoffourreplicateblocksPlotswithinblockswereseparatedby1malleysandblockswereseparatedby5mormoreDetailsofplantestablishmentandmaintenancearegiven inSupportingInformationAppendixS1

23emsp|emspPlant traits affecting arthropod attractiveness

Wedetermined three plant characteristics floral area peak flow-eringweek and flower typewhichwe expectedwould influencearthropodattractivenessTodeterminefloraareawerecordedthenumberoffloralunitscontainingopenflowersineachplotweeklyAfloralunitwasequaltoanindividualflowerinmostcasesbutforAsteraceae species a floral unit was an inflorescence (compositeflower)Flowercountswerealwaysdonewithin1dayofsamplingarthropods(seebelow)Wealsomeasuredthediameter(actinomor-phicorcompositeflowers)orlengthandwidth(zygomorphicflow-ers)offivetotenfloralunitsperplantspeciesandcalculatedfromthesedatatheaveragefloralareaperfloralunitforeachplantspe-cies (Williams etal 2015) This average floral area per floral unitwasmultipliedbythenumberofopenfloralunitsineachploteachweekinordertocalculatethefloralareaperplotWedefinedthepeakfloweringweekforeachplantspeciesastheweeknumberoftheyear thatwascentredon the threeconsecutiveweekshavingthe highest floral area Plant species were also placed into threeflower types actinomorphic composite or zygomorphic flowersPlant species in the familiesFabaceaeLamiaceaePlantaginaceaeandScrophulariaceaehadzygomorphicflowers (n=11)thateitherhaddeepcorollasorrequiredflowerhandlingtoaccessresourcesPlantspecieswithinAsteraceaehadcompositeflowers(n=11)withshortcorollasresultinginaccessibleresourcessplitbetweenmanysmall flowersRemainingplantspecieshadactinomorphic flowerswhich generally offered accessible resourceswith a lower degreeofresourcesplittingcomparedtothecompositeflowersCommonnamesfloweringphenologiesfamiliesandtraitsforeachplantspe-ciesarelistedinSupportingInformationTablesS1andS2

24emsp|emspWild bees and honeybees

Todeterminewildbeeandhoneybeeattractivenesswesampledallplotswithopenflowersweeklybetween0600and1730hrwhentemperatureswereatleast15degCwindwaslow(35msorless)andtheskywasatleastpartlysunnyorbrightlyovercastTocontrolforpotentialdiurnalpatternsinbeevisitationtoflowerseachfloweringplotwassampledtwiceeachweekwiththefirst30sgenerallybeinginthemorningandthesecond30sgenerallybeingintheafternoonofthesamedayHoweverthissometimesvarieddependingontheseasonandfocalplantspeciesForexamplebothweekly30sobser-vationsforMadia elegans and Oenothera elatawereconductedearly


TABLE 1emspAttractivenessof43plantspeciesforfivefunctionalgroupsofarthropodsForeachgroupthemodelestimatedmeannumberofarthropodsper60sofobservation(wildbees

andhoneybees)orper30sofvacuumsampling(herbivorespredatorsandparasiticwasps)ispresentedalongwiththestandarderrors(S

E)ofthemeansPlantspeciesaresortedinorderof

peakbloommonthandthenalphabeticallywithineachmonth

Plan

t spe

cies

Wild

bee

sSE

Hon

eybe

esSE

Her

bivo

res

SEPr

edat

ors

SEPa

rasi

tic w

asps

SE

Amsin

ckia

inte

rmed

ia0

210

11259

093

3694

1371

381

092

521

126

Cala

ndrin

ia m

enzi

esii

062

026

019

012

6379

2482

155

045

281

077

Nem

ophi

la m

acul

ata

004

004

501

174

525

195

149

040

065

022

Nem

ophi

la m

enzi

esii

015

009

468

173

1115

435

344

089

312

083

Phac

elia

cili

ata

163

056

831

325

318

138

033

015

182

056

Achi

llea

mill

efol

ium

060

021

034

017

7673

278

83893

867

1681

387

Colli

nsia

het

erop

hylla

038

015

259

094

1556

606

155

045

095

032

Fago

pyru

m e

scul

entu

m0

000

000

180

111375

533

206

059

134

041

Last

heni

a fr

emon

tii0

72026

051

022

4001

1452

330

082

496

120

Last

heni

a gl

abra

ta0

77032

010

008

8523

3604

138

045

767

212

Lim

nant

hes a

lba

050

019

608

212

3438

1260

215

056

244

063

Lupi

nus m

icro

carp

us d

ensif

loru

s140

044

121

049

1859

721

1337

325

429

112

Lupi

nus s

uccu

lent

us0

80035

031

020

1657

850

1266

405

104

042

Phac

elia

cal

iforn

ica

177

059

1631

644

1308

562

163

052

132

045

Phac

elia

cam

panu

laria

007

007

601

336

221

136

028

016

098

046

Phac

elia

tana

cetif

olia

116

035

1662

567

2697

996

139

039

258

069

Salv

ia c

olum

baria

e005

005

782

308

641

275

407

115

170

055

Spha

eral

cea

ambi

gua

109

034

537

185

2266

828

107

1246

457

112

Trifo

lium

fuca

tum

005

005

000

001

1699

872

467

154

242

087

Trifo

lium

gra

cile

ntum

000

000

015

011

3440

1435

387

109

446

127

Antir

rhin

um c

ornu

tum

119

056

159

094

145

092

034

019

081

039

Clar

kia

purp

urea

004

004

493

171

1289

473

804

188

364

091

Clar

kia

ungu

icul

ata

099

031

4624

1541

624

229

660

155

216

057

Clar

kia

will

iam

soni

i023

011

1627

546

932

341

2616

587

315

080

Erio

phyl

lum

lana

tum

226

064

085

034

3748

1370

2224

501

842

198

Esch

scho

lzia

calif

orni

ca036

015

793

271

1294

473

316

080

455

111

Mon

arde

lla v

illos

a074

025

484

170

915

337

669

160

113

034

Scro

phul

aria

cal

iforn

ica

157

047

642

224

573

214

103

031

159

044

Ascl

epia

s erio

carp

a005

005

074

033

11264

4521

625

166

015

009

Ascl

epia

s fas

cicu

laris

037

017

346

129

19860

7796

449

119

116

037

Cam

isson

iops

is ch

eira

nthi

folia

020

014

384

218

2847

1676

912

338

577

223 (C

ontin

ues)


inthesamedaybecauseflowerscloseinthelatemorningDuringeach 30s observation the number of honeybees visiting flowerswascountedWecaughtanywildbeesvisitingflowerswithahandnetduringthesame30sWepausedtheobservationtimeforhan-dlingspecimenscaughtAnywildbeesescapingthenetwerenotedandare included inanalysesasundeterminedwildbeesEachbeepresentorenteringandvisitingflowerswithintheplotwascountedasanewindividualAnyhoneybeesthatlefttheplotorwildbeesthatescapedthenetandthenreturnedtotheplotagainduringtheobservation might therefore have been counted twice Our sam-plingtimeperplotwaslimitedduetothelargetotalnumberofplotssampledBecausemanagedbumblebeesthatwerepartofanotherexperimentwerepresentatthestudysitein2015(seeabove)bum-blebeeswerenotcollectedin2015Insteadtheywereidentifieddi-rectlyinthefieldeithertogenusorspeciesdependingonobserverNettedwildbeespecimensweredeterminedtospeciesorthelow-esttaxonomiclevelpossibleinthelaboratoryInanalysesweonlyusehoneybeeobservationdataandwildbeenettedspecimendatafromthe3-weekpeakfloweringperiod(definedabove)ofeachplantspecies This resulted in a standardized sampling effort for eachplantspeciesthatalsomatchedthecoverageforherbivorepredatorandparasiticwaspdata(seebelow)Datafromthetwo30sobserva-tionseachweekineachplotandthethreeweeklyobservationsperplotineachyearweresummedbeforeanalysis

25emsp|emspHerbivores predators and parasitic wasps

To determine herbivore predator and parasitic wasp attractive-ness we vacuum sampled all plots with open flowers weekly for30s between 0730 and 1700hr using a modified leaf vacuum(StihlNorfolkVAUSA)Vacuumingtargetedflowersbutincludedupper vegetative parts of the plants close to flowersArthropodswerecollectedinone-gallonfinemeshpaintstrainerbags(TrimacoMorrisvilleNCUSA)placedovertheintakeofthevacuumWevac-uumsampledeitherdirectlyafterbeeobservationswerecompletedoronthefollowingdayusingthesameweathercriteriaas for thebeeobservationsVacuumsampleswerefrozenforlaterprocessinginthelaboratoryWeonlyprocessedsamplesfromthe3-weekpeakfloweringperiod (definedabove)ofeachplantspeciesTaxonomicidentificationofarthropodsinvacuumsampleswasfocusedoniden-tifying three broad functional groups herbivores predators andparasiticwaspsThetaxonomicranktowhichspecimenswereiden-tifiedwastypically tofamilyThisvariedhowever fromtheordertospeciesleveldependingonthevariationoffeedinghabitswithintaxaandourcapacitytoidentifyspecimensfrommultiplearthropodordersWeclassifiedarthropodsincladeswithmainlyplantfeedinghabitsasherbivoresandarthropodsincladeswithmainlypredatoryfeedinghabitsaspredatorsThemostcommonarthropodsnotclas-sifiedintoanyofourfunctionalgroupsweretaxawithomnivorousscavengingorunknownfeedinghabitswithinDipteraColeopteraMiridaeandBerytidae(forspecificationofwhichtaxawithintheseordersandfamiliesweconsideredseeresults)ParasiticwaspswereonlyidentifiedtoasingletaxonomicunitHymenoptera(Parasitica)Pl

ant s

peci

esW

ild b

ees

SEH

oney

bees

SEH

erbi

vore

sSE

Pred

ator

sSE

Para

sitic

was

psSE

Erio

gonu

m fa

scic

ulat

um158

054

881

346

804

343

2650

687

312

091

Gili

a ca

pita

ta086

031

1536

555

252

102

1691

409

142

042

Grin

delia

cam

poru

m498

146

355

133

2993

1157

1390

342

489

126

Hel

iant

hus a

nnuu

s2

11069

597

219

1951

758

558

147

240

066

Lupi

nus f

orm

osus

034

015

027

015

388

156

475

126

082

031

Mal

acot

hrix

saxa

tilis

071

029

380

153

698

299

190

060

128

043

Oen

othe

ra e

lata

027

017

125

076

3187

1915

130

054

106

049

Hel

iant

hus b

olan

deri

302

100

629

250

3215

1343

1704

452

555

153

Hel

iant

hus c

alifo

rnic

us065

023

026

013

243

094

078

025

081

025

Mad

ia e

lega

ns0

000

001135

387

363

136

083

028

178

048

Tric

host

ema

lanc

eola

tum

512

150

083

035

1737

682

1613

400

254

072

Het

erot

heca

gra

ndifl

ora

159

050

113

046

3993

1549

215

064

124

039

TABLE 1emsp(Continued)


Lifestagesconsideredforeachtaxaarespecifiedintheresultssec-tionThethreeweeklysamplesperplotineachyearweresummedbeforeanalysis

26emsp|emspStatistical analyses

WeanalyseddatainSAS94forWindows(SASInstituteIncCaryNC USA) Data transformations described were performed toachieveapproximatelynormaldistributionofmodelresidualswhichwasverifiedbyinspectionsofresidualplots

261emsp|emspAttractiveness across plant species

Weanalysedthenumberofwildbeeshoneybeesherbivorespred-atorsandparasiticwaspssummedperplotandyearingeneralizedlinearmixedmodels (PROCGLIMMIX)withplantspeciesandyearasfixedfactorsandblockasarandomfactorTheln-transformednumberofweeklysampleswasincludedasanoffsetsothattheunitoftheresponsevariablebecamenumberofindividualsper60sofobservationforwildbeesandhoneybeesandper30sofvacuumsampling for herbivores predators and parasitic wasps Adaptivequadraturewasusedasestimationmethodtofacilitatemodelcon-vergenceMeansandstandarderrorsonthescaleofdatawerede-rivedusingtheilinkoptionWedidnotfollow-upoverallsignificanteffects of plant species with any post hoc pairwise comparisonsThiswasbecauseourdatasethadahighnumberofpotentialpair-wisecomparisonsbetweenplantspeciesthateachhadlimitedsta-tisticalpower

262emsp|emspPredictors of plant species attractiveness

Werangenerallinearmodels(PROCGLM)withthemeannumberof wild bees and honeybees (log10 [x+005] transformed) andherbivorespredatorsandparasiticwasps(log10transformed)perplantspeciesasestimatedfromthemixedmodeldescribedaboveasresponsevariablesByusingmodelestimatedmeansasthere-sponsevariableswefocusouranalysesonvariationbetweenandnotwithin plant species in the predictors (van de PolampWright2009) andaccount forunbalancedsamplingeffort forexamplethat not all plant specieswere sampled in both years Predictorvariables were floral area (log10-transformed) peak floweringweekandflowertypeforeachplantspeciesAsingleestimatedmean floral areaandpeak floweringweekperplant specieswasobtainedbyaddingtheseasresponsevariablesinthemixedmodeldescribedinthepreviousparagraphassumingnormaldistributionHowever because peak flowering week was determined at theplantspecies leveleachyearandnot individuallyforeachblockthe model that predicted peak flowering week used data sum-marizedperplant andyear anddidnothaveanyblockeffectAquadraticeffectofbloomperiodwasalsotestedandwasretainedinfinalmodelsifsignificantFloralareaandpeakfloweringweekwerenotcollinear(Pearsoncorrelationr=016p=030varianceinflationfactor=103)butflowertypesdifferedinbloomperiod

(ANOVAF240=571p=00066)withcompositespeciesbloom-ing later than species with actinomorphic flowers (SupportingInformation Figure S1) Flower types also differed in floral area(ANOVAF240=504 p =0011)with specieswith zygomorphicflowers having a lower floral area than species with compositeflowers (Supporting InformationFigureS1)Wethereforealwaystestedtheeffectofflowertypewithfloralareaandpeakfloweringweekincludedinthemodel

263emsp|emspCovariation across arthropod functional groups

To test if arthropod functional group abundances covaried acrossplantspeciesweranpairwisecorrelationtests(PROCCORR)Inputdata were themodel estimatedmean number of wild bees hon-eybees herbivores predators and parasitic wasps for each plantspecies

3emsp |emspRESULTS

In total we sampled 908 wild bees 5209 honeybees 25804herbivores 8009 predators and 2827 parasitic wasps Halictus ligatus Say and B vosnesenskii were the most common wild bees(Supporting Information Table S3) aphids (Aphididae) hoppers(Auchenorrhyncha)andseedbugs(Lygaeidae)werethemostcom-monherbivoresandminutepiratebugs(Anthocoridae)andspiders(Araneae)werethemostcommonpredators(SupportingInformationTableS4)Allarthropod functionalgroupsweresampled inhighernumbers in 2015 compared to in 2016 (wild bees F1241=5517plt000010 honeybees F1241=1383 plt00010 herbivoresF1240=1976p lt000010predatorsF1240=20774p lt 000010 parasiticwaspsF1240=4159plt000010)Totalfloralareaacrossall plant species in the experiment over the sampling seasons isshowninSupportingInformationFigureS2


Attractiveness varied across plant species for all arthropodfunctional groups (wild bees F42241=523 plt000010 hon-eybees F42241=1003 plt000010 herbivores F42240=741plt000010 predators F42240=1616 plt000010 parasiticwaspsF42240=697plt000010)Attractivenessof all plant spe-ciesforeacharthropodfunctionalgroupispresentedinTable1andSupportingInformationFigureS3


Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)


F IGURE 1emsp Influenceofpeakfloweringweekandfloralarea(cmsup2permsup2log10-transformed)onattractivenessof43plantspeciestowildbees(af)honeybees(bg)herbivores(ch)predators(di)andparasiticwasps(ej)Theunitisnumberofindividualsper60sofobservation(log10[x+005]transformed)forwildbeesandhoneybeesandnumberofindividualsper30sofvacuumsampling(log10transformed)forherbivorespredatorsandparasiticwaspsSolidlinesindicatesignificantslopesanddashedlinesindicatenonsignificantslopesNotethatthey-axesrangesvarybyarthropodfunctionalgroup


Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)


Herbivorepredatorandparasiticwaspabundanceswereallposi-tively correlated across plant species (Figure3) Honeybee abun-dancewasnegativelycorrelatedtoherbivoreabundance(Figure3)

4emsp |emspDISCUSSION

Recommendationsofwhichplantspeciestousetosupportbenefi-cialarthropodsareoftenbasedonpersonalexperienceandopinionrather than empirical data (Garbuzov amp Ratnieks 2014) resultingin an unclear evidence base for the recommendations Here weaddress this gap with a data-driven approach that assessed theattractiveness of plants native to California to several function-ally important arthropod groupsWe expand the list ofCalifornianativeplants thatpreviouslyhavebeenassessed forwildbeeandhoneybee attractiveness (Frankie etal 2005) and add informa-tion regardingarthropodgroupswhichareof importance forpestmanagementDetailedrecommendationsofwhichplantspeciestousetosupportfunctionallyimportantarthropodsbasedondatapre-sentedherewilldependonthecroptargeted(egspringfloweringvssummerflowering)andtherelativeimportanceofsupportingdif-ferentgroupsoffunctionallyimportantarthropodsRecentlytoolsforselectingplantsnativetoCaliforniatouseinpollinatorrestora-tionmixeshavebeendeveloped(MrsquoGonigleWilliamsLonsdorfampKremen2017WilliamsampLonsdorf2018)Withthedatapresentedheresuchselectiontoolscanbeextendedtoalsoconsiderarthro-podnaturalenemiesandherbivores

Plantspecieswithahigherfloralareaattractedgreaternumbersofhoneybeespredatorsandparasiticwaspsandtherewasanon-significanttrendinthesamedirectionforwildbeeabundanceThusfloral area measured here as the combination of flower numberandflowersizewithinafixedplotarea (ie floraldisplaydensity)

emergesasasimplemetricthatcanbeusedforplantselectionasit predicts the abundances of several groups of beneficial arthro-podsAlthoughtheseresults inpartaresimilartothoseofFiedlerand Landis (2007b) andTuell etal (2008) they alsodiffer in sev-eral aspects First we found that floral area predicted honeybeeabundancemorestronglythanwildbeeabundancewhereasTuelletal(2008)foundthatfloralareapredictedwildbeebutnothon-eybeeabundanceThisdiscrepancymaybeduetothefactthatourbee communitywasmore strongly dominated by honeybees andto a lesser extent by wild bumblebees whichmight have shiftedinterspecific competition and floral choice (Roubik amp Villanueva-Gutierrez2009)betweenthetwogroupsofbeesSecondwefoundthatattractivenesstoparasiticwaspsgenerallywashighestforplantspecies flowering early in the season and then declined on laterfloweringspecieswhereasFiedlerandLandis(2007b)foundtheop-positeforchalcidparasiticwaspsOurresultmighthavebeendrivenbyparasiticwaspflowervisitationpeakinginlatespring(Figure1e)whentotalflowerabundancereachesitsmaximuminnaturalhabi-tats inCaliforniarsquosMediterraneanclimate(egWilliamsRegetzampKremen2012)

Honeybees preferred actinomorphic over composite flowersThedispersedresourcesofmultifloweredcompositesmightbemoreenergeticallydemandingtoharvestcomparedtolargersingleflow-ers(Carvalheiroetal2014)especiallyforageneralistandrelativelylargespecieslikethehoneybeeCompositeflowersattractedhighernumbers of parasitic wasps compared to actinomorphic flowersHighattractionofparasiticwaspstoAsteraceaehasbeenpreviouslyreported(FiedlerampLandis2007a2007b)despitetheirnarrowandfromtheperspectiveofparasiticwaspsrelativelydeepcorollasthatcanrestricttheiraccesstonectar(egWaumlckers2004)Ithasbeensuggested that nectar poolingmay explain this pattern (FiedlerampLandis2007b)howeverwedidnotmeasurestandingnectar lev-elswithinAsteraceaefloretsFlowertypedidnotexplainwildbeeattractivenessWerecommendthatadditionalfloraltraitssuchasquantityandqualityofnectarandpollen(VaudoTookerGrozingerampPatch2015)beincludedinfuturestudiesastheymaybetterex-plain floral visitationpatternsbywildbeeswhichoftenaremorespecializedflowervisitorsthatalsocanharvestlessaccessiblenec-tarandpollenFurthermore thehoneybee isa singlespeciesbutourwildbeecategoryconsistedofalargesetofspecieswithdiverse

TABLE 2emspStatisticaltestresultsfromgenerallinearmodelswithFvaluesdegreesoffreedom(df)andpvaluesfortheeffectsofbloomperiodbloomperiodsquaredfloralareaandflowertypeonfivearthropodgroups(wildbeeshoneybeesinsectherbivoresarthropodpredatorsandparasiticwasps)Statisticallysignificantresults(plt005)areindicatedinbold

Bloom period Bloom period squared Floral area Flower type

F df p F df P F df p F df p

Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033


morphologiesandlifehistoriesThismeansthattheoverall lackofresponsetofloraltraitsfoundhereforallwildbeescombineddoesnotpreclude floral areaor flower typeas importantpredictorsofplant attractiveness for individual bee species or species groupsHerbivoresdidnotrespondtoanyofthetraitstestedManyherbi-voresinthemostcommongroupslikeaphids(Aphididae)andhop-pers(Auchenorrhyncha)wereprobablyvacuumedfromunderneathorvegetativepartsaroundflowersratherthandirectly fromflow-ersandthislikelyexplainswhytheflowercharacteristicstestednotwereimportantpredictorsoftheirabundance

Thepositivelycorrelatedabundancesofherbivorespredatorsandparasiticwaspsacrossplantspeciesmighthavebeencausedbysharedmechanismsofattractiontoplantsorbyattractionofpredatorsandparasiticwasps toplant species thathosted the largestnumbersoftheirherbivorepreyThetwoexplanationsarenotmutuallyexclusiveThefactthatpredatorandparasiticwaspabundanceswerepositivelycorrelatedtobothfloralareaandherbivoreabundance(whichinitselfwasunrelatedtofloralarea)suggeststhatbothplantandherbivorecuesareimportantfornaturalenemyattractiontoplantsOurresultssuggestthatresourceplantingsfornaturalenemiesneedtoconsiderthe risk of herbivore attraction especially for generalist herbivoresthatalsomaydamagecrops(egMcCabeLoebampGrab2017)Moreunexpectedly the sets of plant species that supported the highestabundances of herbivores also showed lower honeybee attractive-nessAsthemostcommonherbivoregroupsweresap-suckinginsectslikeaphidsandleafhoppersthatdonotdirectlydamageflowersthenegativecorrelationbetween insectherbivoreandhoneybeeabun-dancesmightinsteadhavebeendrivenbyindirectnegativeeffectsonfloralresourcesthroughdecreasedoverallplantquality

Weacknowledge some important limitationsof the approachusedhereFirstitisnotstraightforwardtoclassifyarthropodsintogroupsthateitherarefunctionallyldquodesirablerdquo (egpollinators)orldquoundesirablerdquo (eg herbivores) in agroecosystems (see SaundersPeisley Rader amp Luck 2016) The most important pest speciesamong theherbivoreswill varyheavilydependingonwhatcropsare targeted For example the high herbivore score for narrow-leafmilkweedAsclepias fasciculariswasdrivenbyoleanderaphids(Aphis neriiBoyerdeFonscolombe)whicharenotknownascroppestsinCaliforniaLimitationsofthistypecantosomeextentbeaddressed by considering species-specific interactions betweenplantvisitorsandcandidateresourceplants(egRussoDeBarrosYang SheaampMortensen 2013)whichwas something thatwas

F IGURE 2emsp Influenceofflowertype(Acti=actinomorphicComp=compositeorZygo=zygomorphic)onwildbee(a)honeybee(b)insectherbivore(c)arthropodpredator(d)andparasiticwasp(e)attractivenessFordefinitionsofflowertypesseemaintextTheunitisnumberofindividualsper60sofobservation(log10[x+005]transformed)forwildbeesandhoneybeesandnumberofindividualsper30sofvacuumsampling(log10transformed)forherbivorespredatorsandparasiticwaspsGroupswithdifferentlettersaresignificantlydifferent(plt005)basedonpairwiseposthoccomparisonswithTukeyadjustment


beyond the scope of our study A second limitation is that per-formanceof individualplantspeciesmighthavebeenaffectedbythe local environment such as the soil type and arthropod spe-ciespoolatourstudysiteMostpromisingplantspeciesidentifiedhere should therefore ideallybe further tested inmultiple loca-tionsbothinmonospecificplots(seeRoweGibsonLandisGibbsamp Isaacs2018)aswellas inplantmixesacrossavarietyof localenvironmentsHowever theanalyseswhichexploredplant traitsthatexplainarthropodattractivenessandarthropodcorrelationsinattractivenessusedthe43plantspeciesasreplicatesandarethusmorerobustagainstlackofreplicationatthesitelevelFinallyitisimportanttotestplantsthatarefoundtobeattractivetobeneficialarthropodswiththescreeningapproachusedherewithadditionalon-farmtrialsinordertoassesswhetherhighattractivenessalsotranslates into higher pollination and pest control services deliv-eredtonearbycrops

Ourscreeningoftheattractivenessofnativeplantsforfivefunc-tionallyimportantgroupsofarthropodsindicatesthatresearchonhabitatplantingsforarthropodsbenefitsfromconsideringmultiplepotentialecosystemservicesanddisservicesThismultifunctionalapproachisespeciallyvaluableforthecaseofpollinationbiologi-calpestcontrolandpestdamagewhicharedeliveredbycloselyrelatedorevenpartiallyoverlappinggroupsofarthropodsHabitatmanagementdirectedatoneofthesefunctionalgroupsmayasweillustratealsoaffectotherfunctionalgroupsMultifunctionalhab-itat management therefore must further explore how synergies

between pollination and pest control delivery can be maximizedwhiletrade-offsareminimized

ACKNOWLEDG EMENTS

We thank a large number of assistants in the Williams labora-tory including Bethany Beyer Kitty Bolte Katherine BorchardtAndrew Buderi Staci Cibotti Michael Epperly Lindsey HackChristian Millan Hernandez Haley Schrader and HeatherSpaulding for establishment maintenance and sampling in theexperiment and for identification of arthropods in the labora-tory This publication was supported by the US Departmentof Agriculturersquos (USDA) Agricultural Marketing Service throughGrant16-SCBGP-CA-0035 Its contents are solely the responsi-bilityoftheauthorsanddonotnecessarilyrepresenttheofficialviewsoftheUSDAFundingwasalsoprovidedbyUSDANationalInstituteofFoodandAgriculture(2012-51181-20105-RC1020391to NMW) USDA Natural Resources Conservation Service(68-9104-5-343toKLW)andbyafellowshipfromCarlTryggerFoundationforScientificResearchtoOL

AUTHORSrsquo CONTRIBUTIONS

AllauthorsconceivedtheideasanddesignedmethodologyOLandKLWcollecteddataOLanalysedthedataandledthewritingofthemanuscriptAllauthorscontributedcritically tothedraftsandgavefinalapprovalforpublication

F IGURE 3emspCorrelationmatrixwithr and pvaluesforpairwisecorrelationsbetweenarthropodfunctionalgroupson43plantspeciesshownintheuppertriangleandcorrelationplotsshowninthelowertriangleTheunitisnumberofindividualsper60sofobservation(log10[x+005]transformed)forwildbeesandhoneybeesandnumberofindividualsper30sofvacuumsampling(log10transformed)forherbivorespredatorsandparasiticwaspsStatisticallysignificantresults(plt005)areindicatedinboldSolidlinesindicatesignificantslopesanddashedlinesindicatenonsignificantslopes


DATA ACCE SSIBILIT Y

Data available via the Dryad Digital Repository httpsdoiorg105061dryadc92k731(LundinWardampWilliams2018)

ORCID

Ola Lundin httporcidorg0000-0002-5948-0761

R E FE R E N C E S

BennettEMPetersonGDampGordonLJ (2009)UnderstandingrelationshipsamongmultipleecosystemservicesEcology Letters121394ndash1404httpsdoiorg101111j1461-0248200901387x

BommarcoRKleijnDampPottsSG(2013)EcologicalintensificationHarnessingecosystemservicesforfoodsecurityTrends in Ecology amp Evolution28230ndash238httpsdoiorg101016jtree201210012

Calflora(2017)Calfora Information on California plants for education re-search and conservationBerkeleyCaliforniaTheCalfloraDatabase(anon-profitorganization)Retrievedfromhttpwwwcalfloraorg

Cardinale B J Duffy J E Gonzalez A Hooper D U PerringsC Venail P hellip Naeem S (2012) Biodiversity loss and its im-pact on humanityNature 486 59ndash67 httpsdoiorg101038nature11148

Carvalheiro L G Biesmeijer J C Benadi G Fruumlnd J Stang MBartomeus IhellipKuninWE (2014)Thepotential for indirectef-fectsbetweenco-floweringplantsviasharedpollinatorsdependsonresource abundance accessibility and relatedness Ecology Letters171389ndash1399httpsdoiorg101111ele12342

Chaplin-KramerROrsquoRourkeMEBlitzerEJampKremenC(2011)A meta-analysis of crop pest and natural enemy response tolandscape complexity Ecology Letters 14 922ndash932 httpsdoiorg101111j1461-0248201101642x

FiedlerAKampLandisDA(2007a)AttractivenessofMichigannativeplants toarthropodnaturalenemiesandherbivoresEnvironmental Entomology36751ndash765httpsdoiorg101093ee364751

Fiedler A K amp Landis D A (2007b) Plant characteristics associ-ated with natural enemy abundance at Michigan native plantsEnvironmental Entomology 36 878ndash886 httpsdoiorg101093ee364878

FiedlerAK LandisDAampWratten SD (2008)Maximizing eco-system services from conservation biological control The role ofhabitat management Biological Control 45 254ndash271 httpsdoiorg101016jbiocontrol200712009

Frankie G W Thorp R W Schindler M Hernandez J Ertter Bamp Rizzardi M (2005) Ecological patterns of bees and their hostornamental flowers in two northern California cities Journal of the Kansas Entomological Society 78 227ndash246 httpsdoiorg1023170407081

Garbach K amp Long R F (2017) Determinants of field edge habitatrestoration on farms in Californiarsquos Sacramento Valley Journal of Environmental Management189134ndash141httpsdoiorg101016jjenvman201612036

Garbuzov M amp Ratnieks F L (2014) Listmania The strengths andweaknessesoflistsofgardenplantstohelppollinatorsBioScience641019ndash1026httpsdoiorg101093bioscibiu150

GaribaldiLACarvalheiroLGLeonhardtSDAizenMABlaauwB R Isaacs R hellip Winfree R (2014) From research to actionEnhancing crop yield through wild pollinators Frontiers in Ecology and the Environment12439ndash447httpsdoiorg101890130330

GrabHPovedaKDanforthBampLoebG(2018)Landscapecontextshiftsthebalanceofcostsandbenefitsfromwildflowerborderson

multipleecosystemservicesProceedings of the Royal Society B28520181102httpsdoiorg101098rspb20181102

Isaacs R Tuell J Fiedler A Gardiner M amp Landis D (2009)Maximizing arthropod-mediated ecosystem services in agriculturallandscapes The role of native plants Frontiers in Ecology and the Environment7196ndash203httpsdoiorg101890080035

Klein A M Vaissiere B E Cane J H Steffan-Dewenter ICunninghamSAKremenCampTscharntkeT(2007)Importanceof pollinators in changing landscapes for world crops Proceedings of the Royal Society of London B Biological Sciences274 303ndash313httpsdoiorg101098rspb20063721

KremenCampMilesA(2012)Ecosystemservicesinbiologicallydiver-sifiedversus conventional farming systemsBenefits externalitiesandtrade-offsEcology and Society1740

KremenCWilliamsNMAizenMAGemmill-HerrenBLeBuhnGMinckleyRhellipRickettsTH(2007)Pollinationandothereco-systemservicesproducedbymobileorganismsAconceptualframe-workfortheeffectsofland-usechangeEcology Letters10299ndash314httpsdoiorg101111j1461-0248200701018x

Landis D AWratten S D amp Gurr GM (2000) Habitat manage-menttoconservenaturalenemiesofarthropodpestsinagricultureAnnual Review of Entomology45175ndash201httpsdoiorg101146annurevento451175

Losey J E amp VaughanM (2006) The economic value of ecologicalservices provided by insectsBioScience 56 311ndash323 httpsdoiorg1016410006-3568(2006)56[311TEVOES]20CO2

LundinOWardKLampWilliamsNM(2018)DatafromIdentifyingnativeplantsforcoordinatedhabitatmanagementofarthropodpol-linators herbivores and natural enemies Dryad Digital Repositoryhttpsdoiorg105061dryadc92k731

McCabeELoebGampGrabH (2017)ResponsesofcroppestsandnaturalenemiestowildflowerbordersdependsonfunctionalgroupInsects873httpsdoiorg103390insects8030073

MrsquoGonigleLKWilliamsNMLonsdorfEampKremenC(2017)AtoolforselectingplantswhenrestoringhabitatforpollinatorsConservation Letters10105ndash111httpsdoiorg101111conl12261

MorandinLALongRFampKremenC(2016)Pestcontrolandpolli-nationcostndashbenefitanalysisofhedgerowrestorationinasimplifiedagricultural landscape Journal of Economic Entomology109 1020ndash1027httpsdoiorg101093jeetow086

MorandinLLongRLPeaseCampKremenC(2011)Hedgerowsen-hancebeneficialinsectsonfarmsinCaliforniarsquosCentralValleyJournal of California Agriculture 65 197ndash201 httpsdoiorg103733cav065n04p197

Pisani-GareauT L LetourneauDKampShennanC (2013)Relativedensities of natural enemy and pest insects within Californiahedgerows Environmental Entomology 42 688ndash702 httpsdoiorg101603EN12317

Ricketts T H Regetz J Steffan-Dewenter I Cunningham S AKremenCBogdanskiAhellipVianaBF(2008)LandscapeeffectsoncroppollinationservicesAretheregeneralpatternsEcology Letters11499ndash515httpsdoiorg101111j1461-0248200801157x

Roubik DW amp Villanueva-Gutierrez R (2009) Invasive AfricanizedhoneybeeimpactonnativesolitarybeesApollenresourceandtrapnestanalysisBiological Journal of the Linnean Society98152ndash160httpsdoiorg101111j1095-8312200901275x

Rowe LGibsonD LandisDGibbs Jamp Isaacs R (2018)A com-parisonof drought-tolerantprairieplants to supportmanagedandwild bees in conservation programsEnvironmental Entomology471128ndash1142

Russo L DeBarros N Yang S Shea K amp Mortensen D (2013)Supporting crop pollinators with floral resources Network-basedphenologicalmatchingEcology and Evolution33125ndash3140httpsdoiorg101002ece3703


SaundersMEPeisleyRKRaderRampLuckGW(2016)PollinatorspestsandpredatorsRecognizingecologicaltrade-offsinagroecosys-temsAmbio454ndash14httpsdoiorg101007s13280-015-0696-y

ShackelfordGStewardPRBentonTGKuninWEPottsSGBiesmeijerJCampSaitSM(2013)ComparisonofpollinatorsandnaturalenemiesAmeta-analysisof landscapeandlocaleffectsonabundanceandrichnessincropsBiological Reviews881002ndash1021httpsdoiorg101111brv12040

SidhuCSampJoshiNK(2016)Establishingwildflowerpollinatorhab-itatsinagriculturalfarmlandtoprovidemultipleecosystemservicesFrontiers in Plant Science7363

SutterLAlbrechtMampJeanneretP(2018)LandscapegreeningandlocalcreationofwildflowerstripsandhedgerowspromotemultipleecosystemservicesJournal of Applied Ecology55612ndash620httpsdoiorg1011111365-266412977

TamburiniGDeSimoneSSiguraMBoscuttiFampMariniL(2016)Soilmanagementshapesecosystemserviceprovisionandtrade-offsinagriculturallandscapesProceedings of the Royal Society of London B Biological Sciences 283 20161369 httpsdoiorg101098rspb20161369

TuellJKFiedlerAKLandisDampIsaacsR(2008)Visitationbywildand managed bees (Hymenoptera Apoidea) to eastern US nativeplantsforuse inconservationprogramsEnvironmental Entomology37 707ndash718 httpsdoiorg1016030046-225X(2008)37[707VBWAMB]20CO2

UCIPM(2018)WeedphotogalleryUniversityofCaliforniaAgricultureamp Natural Resources Statewide Integrated Pest ManagementProgram Retrieved from httpipmucanreduPMGweeds_introhtml

USDA NRCS (2017) Web Soil Survey United States Department ofAgriculture Natural Resources Conservation Service Retrievedfromhttpwebsoilsurveyscegovusdagov

vandePolMampWrightJ(2009)Asimplemethodfordistinguishingwithin-versusbetween-subjecteffectsusingmixedmodelsAnimal Behaviour77753ndash758

vanRijnPCampWaumlckersFL (2016)Nectaraccessibilitydeterminesfitnessflowerchoiceandabundanceofhoverfliesthatprovidenat-uralpestcontrolJournal of Applied Ecology53925ndash933httpsdoiorg1011111365-266412605

VansellGH(1941)NectarandpollenplantsofCaliforniaUniversityofCaliforniaAgriculturalExperimentStationBulletin517

VaudoADTookerJFGrozingerCMampPatchHM(2015)Beenutrition and floral resource restoration Current Opinion in Insect Science10133ndash141httpsdoiorg101016jcois201505008

Waumlckers F L (2004) Assessing the suitability of flowering herbs asparasitoid food sources Flower attractiveness and nectar acces-sibility Biological Control 29 307ndash314 httpsdoiorg101016jbiocontrol200308005

Williams N M amp Lonsdorf E (2018) Selecting cost-effective plantmixestosupportpollinatorsBiological Conservation217195ndash202httpsdoiorg101016jbiocon201710032

Williams N M Regetz J amp Kremen C (2012) Landscape-scaleresources promote colony growth but not reproductive per-formance of bumble bees Ecology 93 1049ndash1058 httpsdoiorg10189011-10061

Williams N MWard K L Pope N Isaacs R Wilson J May EA hellip Peters J (2015) Native wildflower plantings support wildbee abundance and diversity in agricultural landscapes across theUnited States Ecological Applications 25 2119ndash2131 httpsdoiorg10189014-17481

Wratten SDGillespieMDecourtyeAMader EampDesneuxN(2012) Pollinator habitat enhancement Benefits to other ecosys-tem servicesAgriculture Ecosystems amp Environment159 112ndash122httpsdoiorg101016jagee201206020

XercesSociety(2018)PollinatorPlantsCaliforniaTheXercesSocietyfor Invertebrate Conservation Retrieved from httpsxercesorgpollinator-conservationplant-listspollinator-plants-california

Zhang W Ricketts T Kremen C Carney K amp Swinton S M(2007) Ecosystem services and dis-services to agricultureEcological Economics 64 253ndash260 httpsdoiorg101016jecolecon200702024

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleLundinOWardKLWilliamsNMIdentifyingnativeplantsforcoordinatedhabitatmanagementofarthropodpollinatorsherbivoresandnaturalenemies J Appl Ecol 2018001ndash12 httpsdoiorg1011111365-266413304


1emsp |emspINTRODUC TION

Integration of functionally important biodiversity and associatedecosystemservicesintocropproductionisimportantforthelong-term sustainability of agricultural systems (Cardinale etal 2012Kremen amp Miles 2012) Crop pollinators and natural enemies tocroppestsaretwoprimaryexamplesofsuchfunctionalbiodiversitythathave receivedparticularattention (Kleinetal2007LoseyampVaughan2006)Increaseduseofthesesupportingecosystemser-viceshasthepotentialtoreduceanthropogenicinputstoagriculturesuch as pesticides and intensive honeybee keeping practices andtherebycontributetosustainableagriculture (BommarcoKleijnampPotts 2013)Despite great potential the ability to integrate sup-portingecosystemservices intocropproduction isconstrainedbylimitedguidanceonhowthiscanbeachievedinpracticeThechal-lengeismagnifiedwhenmultipleservicesaresoughtsimultaneouslyaspotentialtrade-offsmarginalgainsandlossesmustbeconsidered(BennettPetersonampGordon2009TamburiniDeSimoneSiguraBoscuttiampMarini2016)

Croppollinationandpestcontrolaremobile-agent-basedecosys-temservices(Kremenetal2007)andinthecaseofpestdamagemdashdisservices (Zhang Ricketts Kremen Carney amp Swinton 2007)andas such theorganisms responsible fordelivering themcanbeaffectedbysimilarenvironmentaldrivers(Shackelfordetal2013)Naturalandsemi-naturalhabitats intheagricultural landscapeforexamplepromotebothpollinators(Rickettsetal2008)andnaturalenemiestocroppests(Chaplin-KramerOrsquoRourkeBlitzerampKremen2011)Managingforcroppollinationandpestcontrolprovidedbyarthropods in agriculture often entails actions that provide foodnesting or overwintering habitat and protection from agriculturaldisturbancefor thetargetserviceproviders (Garibaldietal2014LandisWratten ampGurr 2000)Management actions to promotepollinatorsandnaturalenemieshavehoweverlargelybeendevel-opedseparatelyandthepossibleeffectsoninsectherbivoressuchascroppestshaveoftenbeenoverlookedHabitatswithfloweringresources forexamplearetypicallyestablishedeitherforpollina-torsor fornaturalenemiesalthougheachof theseplanting typesmayaffectbothorganismgroups(FiedlerLandisampWratten2008WrattenGillespieDecourtyeMaderampDesneux2012)Therehasbeen limited effort to integrate provision of flowering resourcesforpollinationandpestcontrol(butseeGrabPovedaDanforthampLoeb2018SutterAlbrechtampJeanneret2018)Thisissurprisinggiventhatforgrowersitisimportantthatplantingsforpollinatorsdonotincreasepestpressureanddesirablethattheyprovidebiologicalpestcontrolservices(SidhuampJoshi2016)Consideringpollinationandpestcontrolservicesintandemalsohasgreatpotentialtomakehabitatplantingsmorecosteffectiveandincreasethelikelihoodof

adoption(GarbachampLong2017MorandinLongampKremen2016)Afirstcriticalsteptowardsdesignandimplementationofmultifunc-tionalplantingsisidentificationofsuitableplantspeciestousethatsupportpollinatorsandnaturalenemiesbutnotpests

Nativeplantsinparticularshowpromiseforuseinhabitatman-agement for pollinators and natural enemies as they are adaptedforgrowingunderlocalconditionsandarelesslikelytobeinvasive(FiedlerampLandis2007a IsaacsTuell FiedlerGardinerampLandis2009)Useofnativeplantshoweveralsocomplicatesplantchoicebecauseplantspeciesthataresuitableforpropagationandattrac-tiveforarthropodsneedtobeidentifiedinaregion-specificmannerTheprocessofselectingplantspeciesformultifunctionality isfur-thercomplicatedbecausethebestspeciesforsupportingpollinatorsmay ormay not support natural enemies and vice versa and fur-thermoretrade-offsbetweenbenefitingbeneficialarthropodsandpromotingpestsmustbeconsideredThisselectionprocesswouldbegreatlyfacilitatedifkeyplanttraitscouldbe identifiedthatareassociatedwithpollinatorherbivoreandnaturalenemyattractive-nessStudiesofplantsnativetoMichigan(US)showedthatthetim-ingofpeakbloomandfloralareawerepositivelyrelatedtonaturalenemyabundance (FiedlerampLandis2007a2007b)Bloomperiodand floral areawere also positively related to the abundance anddiversityofwildbeesvisitingplantswhereasfloralareawasunre-latedtotheabundanceofhoneybees(TuellFiedlerLandisampIsaacs2008)Apartfrombloomperiodandfloralareatheaccessibilityofresources(nectarandpollen)toarthropodsisalsolikelytoinfluenceattractivenessResourceaccessibilityisdrivenbyseveralinteractingfactorsincludingcorollawidthanddepthwhetherresourcesareof-feredinlargevsmanysmallflowers(egcompositeinflorescencesinAsteraceae)andarthropodbodyandmouthpartsize(Carvalheiroetal2014vanRijnampWaumlckers2016Waumlckers2004)Suchmul-tivariate interaction complicates selection of a single informativeflowertraitIthasnotbeentestedwhetherflowertype(actinomor-phic compositeor zygomorphic flowers) couldserveasageneralproxy for a set of interacting factors affecting arthropod attrac-tiveness Actinomorphic and composite flowers generally presentmoreaccessibleresourceswithlessandmoresplittingofresourcesbetweenflowersrespectivelywhilezygomorphicflowersgenerallyhave less accessible resources due to deeper corollas or specificflowerhandlingrequiredtoaccessresources

The overall aim of our studywas to identify California nativeplantsandmoregenerallyplanttraitssuitableforcoordinatedhab-itatmanagement of arthropodpollinators herbivores andnaturalenemiesandpromoteintegratedecosystemservicesinagriculturallandscapesMorespecificallyweask(a)whichnativeplantsamongourcandidatesetattractthehighestabundancesofwildbeeshon-eybees herbivores predators and parasiticwasps (b) if the total

K E Y W O R D S

biologicalcontrolhoneybeemultifunctionalitynativebeenaturalenemyparasiticwasppollinatorwildbee


















Plan

t spe

cies

Wild

bee

sSE

Hon

eybe

esSE

Her

bivo

res

SEPr

edat

ors

SEPa

rasi

tic w

asps

SE

Amsin

ckia

inte

rmed

ia0

210

11259

093

3694

1371

381

092

521

126

Cala

ndrin

ia m

enzi

esii

062

026

019

012

6379

2482

155

045

281

077

Nem

ophi

la m

acul

ata

004

004

501

174

525

195

149

040

065

022

Nem

ophi

la m

enzi

esii

015

009

468

173

1115

435

344

089

312

083

Phac

elia

cili

ata

163

056

831

325

318

138

033

015

182

056

Achi

llea

mill

efol

ium

060

021

034

017

7673

278

83893

867

1681

387

Colli

nsia

het

erop

hylla

038

015

259

094

1556

606

155

045

095

032

Fago

pyru

m e

scul

entu

m0

000

000

180

111375

533

206

059

134

041

Last

heni

a fr

emon

tii0

72026

051

022

4001

1452

330

082

496

120

Last

heni

a gl

abra

ta0

77032

010

008

8523

3604

138

045

767

212

Lim

nant

hes a

lba

050

019

608

212

3438

1260

215

056

244

063

Lupi

nus m

icro

carp

us d

ensif

loru

s140

044

121

049

1859

721

1337

325

429

112

Lupi

nus s

uccu

lent

us0

80035

031

020

1657

850

1266

405

104

042

Phac

elia

cal

iforn

ica

177

059

1631

644

1308

562

163

052

132

045

Phac

elia

cam

panu

laria

007

007

601

336

221

136

028

016

098

046

Phac

elia

tana

cetif

olia

116

035

1662

567

2697

996

139

039

258

069

Salv

ia c

olum

baria

e005

005

782

308

641

275

407

115

170

055

Spha

eral

cea

ambi

gua

109

034

537

185

2266

828

107

1246

457

112

Trifo

lium

fuca

tum

005

005

000

001

1699

872

467

154

242

087

Trifo

lium

gra

cile

ntum

000

000

015

011

3440

1435

387

109

446

127

Antir

rhin

um c

ornu

tum

119

056

159

094

145

092

034

019

081

039

Clar

kia

purp

urea

004

004

493

171

1289

473

804

188

364

091

Clar

kia

ungu

icul

ata

099

031

4624

1541

624

229

660

155

216

057

Clar

kia

will

iam

soni

i023

011

1627

546

932

341

2616

587

315

080

Erio

phyl

lum

lana

tum

226

064

085

034

3748

1370

2224

501

842

198

Esch

scho

lzia

calif

orni

ca036

015

793

271

1294

473

316

080

455

111

Mon

arde

lla v

illos

a074

025

484

170

915

337

669

160

113

034

Scro

phul

aria

cal

iforn

ica

157

047

642

224

573

214

103

031

159

044

Ascl

epia

s erio

carp

a005

005

074

033

11264

4521

625

166

015

009

Ascl

epia

s fas

cicu

laris

037

017

346

129

19860

7796

449

119

116

037

Cam

isson

iops

is ch

eira

nthi

folia

020

014

384

218

2847

1676

912

338

577

223 (C

ontin

ues)





ant s

peci

esW

ild b

ees

SEH

oney

bees

SEH

erbi

vore

sSE

Pred

ator

sSE

Para

sitic

was

psSE

Erio

gonu

m fa

scic

ulat

um158

054

881

346

804

343

2650

687

312

091

Gili

a ca

pita

ta086

031

1536

555

252

102

1691

409

142

042

Grin

delia

cam

poru

m498

146

355

133

2993

1157

1390

342

489

126

Hel

iant

hus a

nnuu

s2

11069

597

219

1951

758

558

147

240

066

Lupi

nus f

orm

osus

034

015

027

015

388

156

475

126

082

031

Mal

acot

hrix

saxa

tilis

071

029

380

153

698

299

190

060

128

043

Oen

othe

ra e

lata

027

017

125

076

3187

1915

130

054

106

049

Hel

iant

hus b

olan

deri

302

100

629

250

3215

1343

1704

452

555

153

Hel

iant

hus c

alifo

rnic

us065

023

026

013

243

094

078

025

081

025

Mad

ia e

lega

ns0

000

001135

387

363

136

083

028

178

048

Tric

host

ema

lanc

eola

tum

512

150

083

035

1737

682

1613

400

254

072

Het

erot

heca

gra

ndifl

ora

159

050

113

046

3993

1549

215

064

124

039













3emsp |emspRESULTS




















Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033










ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S








































































Plan

t spe

cies

Wild

bee

sSE

Hon

eybe

esSE

Her

bivo

res

SEPr

edat

ors

SEPa

rasi

tic w

asps

SE

Amsin

ckia

inte

rmed

ia0

210

11259

093

3694

1371

381

092

521

126

Cala

ndrin

ia m

enzi

esii

062

026

019

012

6379

2482

155

045

281

077

Nem

ophi

la m

acul

ata

004

004

501

174

525

195

149

040

065

022

Nem

ophi

la m

enzi

esii

015

009

468

173

1115

435

344

089

312

083

Phac

elia

cili

ata

163

056

831

325

318

138

033

015

182

056

Achi

llea

mill

efol

ium

060

021

034

017

7673

278

83893

867

1681

387

Colli

nsia

het

erop

hylla

038

015

259

094

1556

606

155

045

095

032

Fago

pyru

m e

scul

entu

m0

000

000

180

111375

533

206

059

134

041

Last

heni

a fr

emon

tii0

72026

051

022

4001

1452

330

082

496

120

Last

heni

a gl

abra

ta0

77032

010

008

8523

3604

138

045

767

212

Lim

nant

hes a

lba

050

019

608

212

3438

1260

215

056

244

063

Lupi

nus m

icro

carp

us d

ensif

loru

s140

044

121

049

1859

721

1337

325

429

112

Lupi

nus s

uccu

lent

us0

80035

031

020

1657

850

1266

405

104

042

Phac

elia

cal

iforn

ica

177

059

1631

644

1308

562

163

052

132

045

Phac

elia

cam

panu

laria

007

007

601

336

221

136

028

016

098

046

Phac

elia

tana

cetif

olia

116

035

1662

567

2697

996

139

039

258

069

Salv

ia c

olum

baria

e005

005

782

308

641

275

407

115

170

055

Spha

eral

cea

ambi

gua

109

034

537

185

2266

828

107

1246

457

112

Trifo

lium

fuca

tum

005

005

000

001

1699

872

467

154

242

087

Trifo

lium

gra

cile

ntum

000

000

015

011

3440

1435

387

109

446

127

Antir

rhin

um c

ornu

tum

119

056

159

094

145

092

034

019

081

039

Clar

kia

purp

urea

004

004

493

171

1289

473

804

188

364

091

Clar

kia

ungu

icul

ata

099

031

4624

1541

624

229

660

155

216

057

Clar

kia

will

iam

soni

i023

011

1627

546

932

341

2616

587

315

080

Erio

phyl

lum

lana

tum

226

064

085

034

3748

1370

2224

501

842

198

Esch

scho

lzia

calif

orni

ca036

015

793

271

1294

473

316

080

455

111

Mon

arde

lla v

illos

a074

025

484

170

915

337

669

160

113

034

Scro

phul

aria

cal

iforn

ica

157

047

642

224

573

214

103

031

159

044

Ascl

epia

s erio

carp

a005

005

074

033

11264

4521

625

166

015

009

Ascl

epia

s fas

cicu

laris

037

017

346

129

19860

7796

449

119

116

037

Cam

isson

iops

is ch

eira

nthi

folia

020

014

384

218

2847

1676

912

338

577

223 (C

ontin

ues)





ant s

peci

esW

ild b

ees

SEH

oney

bees

SEH

erbi

vore

sSE

Pred

ator

sSE

Para

sitic

was

psSE

Erio

gonu

m fa

scic

ulat

um158

054

881

346

804

343

2650

687

312

091

Gili

a ca

pita

ta086

031

1536

555

252

102

1691

409

142

042

Grin

delia

cam

poru

m498

146

355

133

2993

1157

1390

342

489

126

Hel

iant

hus a

nnuu

s2

11069

597

219

1951

758

558

147

240

066

Lupi

nus f

orm

osus

034

015

027

015

388

156

475

126

082

031

Mal

acot

hrix

saxa

tilis

071

029

380

153

698

299

190

060

128

043

Oen

othe

ra e

lata

027

017

125

076

3187

1915

130

054

106

049

Hel

iant

hus b

olan

deri

302

100

629

250

3215

1343

1704

452

555

153

Hel

iant

hus c

alifo

rnic

us065

023

026

013

243

094

078

025

081

025

Mad

ia e

lega

ns0

000

001135

387

363

136

083

028

178

048

Tric

host

ema

lanc

eola

tum

512

150

083

035

1737

682

1613

400

254

072

Het

erot

heca

gra

ndifl

ora

159

050

113

046

3993

1549

215

064

124

039













3emsp |emspRESULTS




















Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033










ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S



























































ant s

peci

esW

ild b

ees

SEH

oney

bees

SEH

erbi

vore

sSE

Pred

ator

sSE

Para

sitic

was

psSE

Erio

gonu

m fa

scic

ulat

um158

054

881

346

804

343

2650

687

312

091

Gili

a ca

pita

ta086

031

1536

555

252

102

1691

409

142

042

Grin

delia

cam

poru

m498

146

355

133

2993

1157

1390

342

489

126

Hel

iant

hus a

nnuu

s2

11069

597

219

1951

758

558

147

240

066

Lupi

nus f

orm

osus

034

015

027

015

388

156

475

126

082

031

Mal

acot

hrix

saxa

tilis

071

029

380

153

698

299

190

060

128

043

Oen

othe

ra e

lata

027

017

125

076

3187

1915

130

054

106

049

Hel

iant

hus b

olan

deri

302

100

629

250

3215

1343

1704

452

555

153

Hel

iant

hus c

alifo

rnic

us065

023

026

013

243

094

078

025

081

025

Mad

ia e

lega

ns0

000

001135

387

363

136

083

028

178

048

Tric

host

ema

lanc

eola

tum

512

150

083

035

1737

682

1613

400

254

072

Het

erot

heca

gra

ndifl

ora

159

050

113

046

3993

1549

215

064

124

039













3emsp |emspRESULTS




















Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033










ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S


































































3emsp |emspRESULTS




















Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033










ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S





































































Wildbees 296 138 0093 020 137 065 385 138 0057 081 238 045

Honeybees 255 138 012 139 137 025 810 138 00071 649 238 00038

Herbivores 015 138 070 029 137 059 102 138 032 191 238 016

Predators 083 138 037 238 137 013 560 138 0023 067 238 052

Parasiticwasps 856 138 00058 009 137 077 562 138 0023 374 238 0033










ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S
































































ACKNOWLEDG EMENTS








ORCID


R E FE R E N C E S


























































ORCID


R E FE R E N C E S























































Identifying native plants for coordinated habitat ...€¦ · Natural and semi-natural habitats in...

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Transcript of Identifying native plants for coordinated habitat ...€¦ · Natural and semi-natural habitats in...