identifying native plants for coordinated habitat ...€¦ · natural and semi-natural habitats in...
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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
4emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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)
emspensp emsp | emsp5Journal of Applied EcologyLUNDIN et aL
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)
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
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
4emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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)
emspensp emsp | emsp5Journal of Applied EcologyLUNDIN et aL
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)
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
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
4emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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)
emspensp emsp | emsp5Journal of Applied EcologyLUNDIN et aL
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)
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
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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
4emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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)
emspensp emsp | emsp5Journal of Applied EcologyLUNDIN et aL
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)
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp5Journal of Applied EcologyLUNDIN et aL
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)
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
6emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
31emsp|emspAttractiveness across plant species
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
32emsp|emspPredictors of plant species attractiveness
Theabundancesofhoneybeespredatorsandparasiticwaspswereall positively affected by floral area with a nonsignificant trendin the same direction for wild bees (Figure1fgij Table2) Laterbloomperiodwasassociatedwithfewerparasiticwasps(Figure1eTable2)Herbivoreswerenotaffectedbyeitherfloralareaorbloomperiod(Figure1chTable2)
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp7Journal of Applied EcologyLUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
8emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
Actinomorphic flowers were more attractive than compositeflowers tohoneybeeswhilecomposite flowersweremoreattrac-tive than actinomorphic flowers to parasitic wasps (Figure2beTable2)Otherarthropodgroups showednosignificantattractiontoeitherflowertype(Figure2Table2)
33emsp|emspCovariation across arthropod functional groups
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp9Journal of Applied EcologyLUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
10emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
emspensp emsp | emsp11Journal of Applied EcologyLUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
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
12emsp |emsp emspenspJournal of Applied Ecology LUNDIN et aL
SaundersMEPeisleyRKRaderRampLuckGW(2016)PollinatorspestsandpredatorsRecognizingecologicaltrade-offsinagroecosys-temsAmbio454ndash14httpsdoiorg101007s13280-015-0696-y
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SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleLundinOWardKLWilliamsNMIdentifyingnativeplantsforcoordinatedhabitatmanagementofarthropodpollinatorsherbivoresandnaturalenemies J Appl Ecol 2018001ndash12 httpsdoiorg1011111365-266413304