Delaying Onion Planting to Control Onion Maggot (Diptera: Anthomyiidae)

12 Pages·2016·0.49 MB·English

Delaying Onion Planting to Control Onion Maggot (Diptera:
Anthomyiidae): Efficacy and Underlying Mechanisms
Author(s): Brian A. Nault, Benjamin P. Werling, Richard W. Straub, and Jan P.
Nyrop
Source: Journal of Economic Entomology, 104(5):1622-1632.
Published By: Entomological Society of America
DOI: http://dx.doi.org/10.1603/EC11175
URL: http://www.bioone.org/doi/full/10.1603/EC11175
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the
biological, ecological, and environmental sciences. BioOne provides a sustainable online
platform for over 170 journals and books published by nonprofit societies, associations,
museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates
your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial
use. Commercial inquiries or rights and permissions requests should be directed to the
individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers,
academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
HORTICULTURALENTOMOLOGY
Delaying Onion Planting to Control Onion Maggot (Diptera:
Anthomyiidae): Efficacy and Underlying Mechanisms
BRIANA.NAULT,1,2BENJAMINP.WERLING,1RICHARDW.STRAUB,3ANDJANP.NYROP1
J.Econ.Entomol.104(5):1622Ð1632(2011);DOI:http://dx.doi.org/10.1603/EC11175
ABSTRACT Onionmaggot,Deliaantiqua(Meigen)(Diptera:Anthomyiidae),isanimportantpestof
onion,AlliumcepaL.,innortherntemperateareas,especiallyintheGreatLakesregionofNorthAmerica.
ManagementofD.antiquareliesoninsecticideuseatplanting,butinsecticideresistancecancausecontrol
failuresthatthreatenthelong-termviabilityofthisstrategy.Delayingthetimeonionsareplantedwas
investigatedasanalternativemanagementapproachforD.antiquaandtheecologicalandbehavioral
mechanismsunderlyinghostageandinsectrelationshipswereexaminedinlaboratoryandÞeldexperi-
ments.Delayingonionplantingbytwotofourweeksreduceddamagetoonionsby35and90%,respectively.
Onionsplantedlateremergedlaterandthisreducedtheperiodoverwinteredßieshadtoovipositonthe
plants.Moreover,ßiestendedtolayfewtonoeggsontheseyoung,late-plantedonions.Asanticipated,
D.antiqualaid4Ð8timesmoreeggsonolderonionsthanonyoungonions,andolderonionsweremore
resilienttoinjurycausedbyD.antiquaneonatescomparedwithyoungeronions.However,theresiliency
tomaggotattacklessenedasthedensityofD.antiquaincreasedfrom2to10eggsperplant,whichprobably
explainswhygreaterlevelsofmaggotdamagearetypicallyobservedinearlyonionplantingscompared
withlaterplantings.Delayingonionplantinguntilmid-MayreducedD.antiquadamagewithoutjeopar-
dizingtheperiodrequiredtoproducemarketableyield,butthisculturaltacticmustbecombinedwith
othermanagementstrategiestopreventeconomicloss.
KEYWORDS Deliaantiqua,oviposition,Alliumcepa,plantingdate,culturalcontrol
Onion, Allium cepa L., is a high-value specialty crop unmarketable (Hoffmann et al. 1996). Management
grown throughout the Great Lakes region of North effortsprimarilytargettheÞrstgeneration.
America.Onionsgrowninthisregionarelong-day,globe Insecticideusecontinuestobetheprincipaltactic
types(Hoffmannetal.1996)thatmaturebetween90and for D. antiqua control (Eckenrode and Nyrop 1995,
115dafterplantinginAprilandearlyMay.Bulbsare Nault et al. 2006a), primarily because it has been
harvested between July and October. In this region, reliable,easytoimplement,andisrelativelyinexpen-
onionsaretypicallygrownonhigh-organicmucksoils, sive.Formanyyears,growershavereliedononlytwo
which are geographically isolated areas located in insecticides,chlorpyrifosandcyromazine(Tayloret
drainedlakebeds.Oniongrowersoftendonotrotate al.2001).Chlorpyrifosisappliedasadrenchtreatment
onionÞelds,andthislackofrotationexacerbatesprob- inthefurrowatplanting,andonionseediscommer-
lemswithplantpathogensandinsects. ciallytreatedwithcyromazine.ControlofD.antiqua
Onion maggot, Delia antiqua (Meigen) (Diptera: populationswithchlorpyrifoshasbecomeunpredict-
Anthomyiidae), is one of the most serious pests of ablebecausemanypopulationshavedevelopedresis-
onion in the Great Lakes region. There are three tancetoit(Naultetal.2006b),leavingcyromazineas
generationsofD.antiquaperyear(Eckenrodeetal. the only effective option. Recently, new seed treat-
1975), but the Þrst generation causes the greatest ments have been identiÞed to control D. antiqua
economiclossbecauselarvaekillyoungonionplants. (Nault et al. 2006a), and two will become commer-
Onion plant stands can be reduced by at least half ciallyavailablein2011:thecombinationofclothiani-
whenleftunprotected(Tayloretal.2001,Naultetal. din and imidacloprid (Sepresto 75WS, Bayer Crop-
2006a). Second- and third-generation larvae cause Science, Research Triangle Park, NC) and the
verylittledamagetotheonioncroprelativetotheÞrst combination of spinosad, thiamethoxam and several
generation, but feeding injury can distort bulbs and fungicides (FarMore FI500, Syngenta Crop Protec-
allowentrybypathogens,bothofwhichrenderonions tion,Greensboro,NC).Long-termmanagementofD.
antiqua should not rely exclusively on use of these
1DepartmentofEntomology,NewYorkStateAgriculturalExperi- insecticides if they are to remain effective (Loosjes
mentStation,CornellUniversity,630W.NorthSt.,Geneva,NY14456. 1976).
2Correspondingauthor,e-mail:[email protected]. Delaying onion planting into late spring has long
3DepartmentofEntomology,NewYorkStateAgriculturalExper-
beensuggestedasamethodofculturalcontrolforD.
imentStation,HudsonValleyLaboratory,CornellUniversity,3357
Route9W,Highland,NY12528. antiqua(DoaneandChapman1952),butitsefÞcacy
0022-0493/11/1622Ð1632$04.00/0(cid:2)2011EntomologicalSocietyofAmerica
October2011 NAULTETAL.:ONIONPLANTAGEIMPACTSONONIONMAGGOT 1623
has not been evaluated. Theoretically, this strategy aregrowninOrangeCounty(southeast),30%inOs-
wouldallowtheonioncroptoescapeinfestationby wego, Wayne and Yates counties (central), and the
reducingthetimeplantswouldbeexposedtoovipo- remainderinOrleansandGenesseecounties(west).
sitioninthespring.Yet,pastresearchhasshownthat Weed,disease,andThripstabaciLindemanmanage-
onionsbecomemoreresilienttoD.antiquaattackas mentwerefollowedasrecommendedbyReinersand
they grow older. For example, Finch et al. (1986a) Petzoldt (2011). Insecticides targeting thrips rarely
foundthat37%ofD.antiquaeggsplacedontoearly- affectD.antiquapopulationsbecausetheyareapplied
bulbingonionplantssurvivedtopupation,whereasno attheendoftheÞrstD.antiquagenerationandfoliar
pupae were produced on plants that were 3Ð5 wk insecticidesprayshaveminimalimpactonßymortal-
older.Incontrasttotherecommendationofplanting ity(Finchetal.1986b).
latetoavoidD.antiquaattack(DoaneandChapman TherelationshipbetweenplantingdateandD.an-
1952),theseresultssuggestthatitmaybepreferable tiquadamagewasinvestigatedfrom2003through2005
forgrowerstoplantonionsearlyintheseasonsothat atÞeldsitesmentionedabove.The2004experiment
onionsareasoldaspossible,andthusmaximallyre- alsocomparedplantdamagelevelsbetweeninsecti-
silient,whenD.antiquaemergeandoviposit. cide-andnoninsecticidetreatedonions,whereasone
DamagebyD.antiquatendstobegreaterinearly- ofthe2005experimentscompareddamagelevelsbe-
plantedonionÞeldsthaninlate-plantedonionÞelds. tweenearly-andlate-maturing,long-dayonionculti-
Thus,somefactormustcausetheinherentresiliency vars.
of older plants to D. antiqua attack to break down. 2003 Planting Date Experiment. This experiment
Early-plantedonionsarelargerthanlate-plantedon- was conducted near Potter, NY, in Yates County.
ionsatthetimeD.antiquaovipositionoccurs.Inlab- Therewerethreeplantingdatesconsideredasearly
oratoryexperiments,femaleD.antiqualaymoreeggs (16 April), mid (6 May), and late (28 May) for the
onlargerplantswhenofferedachoicebetweenthese onionplantingperiodinthisregion.ÔMillenniumÕon-
and smaller plants (Harris et al. 1987). Although a ionseedswereplantedinsinglerowplotsthatwere
laboratory choice test with single plants is not the 7.6minlengthandseparatedfromotherrowsby38
sameascomparingovipositionchoicesinÞeldswith cm. Seeds were planted at a density of 30 per m by
differentagedonions,femaleD.antiquamaylaymore using a hand-pushed cone seeder equipped with a
eggsonlarger,early-plantedonions.Thus,densitiesof gravity-fed system for in-furrow drenches of pesti-
Þrst-generation D. antiqua eggs might be greater on cides,mountedontoaPlanetJr.frame.Eachplanting
early-thanonlate-plantedonions,providingabehav- date treatment was arranged in a randomized com-
ioralexplanationforelevateddamage. pleteblockdesignreplicatedsixtimes.Seedswerenot
The purpose of this research was to determine treatedwithinsecticides,butweretreatedwithfun-
whetherD.antiquadamagecouldbereducedbydelay- gicides to manage seedling diseases. This was done
ingonionplanting.Inaddition,weaimedtoidentifythe using a solution containing a Þlm-forming polymer
mechanismsthatunderlievariationinD.antiquadamage (Disco,A1.018.IncotecInc.,Salinas,CA)thatencap-
withplantingdate.Toaccomplishthis,weusedacom- sulatedtheseedwithapreciseamountofthiramand
binationofÞeldandlaboratoryexperiments.Fieldex- carboxin(Pro-Gro)atarateof2.0g(AI)/100g(see
perimentsfocusedonquantifyingdifferencesinD.an- Taylor 2003). Additional protection against diseases
tiquadamagebetweenonionsplantedatdifferentdates was afforded with a drench treatment of mancozeb
andrelatingdifferencestoactivityofovipositingadults. (DithaneF-45,DowAgroSciences,Indianapolis,IN)
Laboratorystudiesfocusedondetermining1)howovi- atarateof5.6liters/ha.
positionmightbeaffectedbyexposingßiestoarangeof ThenumberofplantsdeadordyingfromD.antiqua
plantagesforvaryingperiodsand2)howtheinherent feeding was recorded one or two times per week
resistanceofdifferent-agedplantsinteractswithD.an- beginninginlateMayandendinginJulyattheendof
tiqua larval densities. We hypothesized that 1) plant theÞrstlarvalgeneration.Seedlingscontainingmag-
damagewouldbereducedbyplantingonionslaterinthe gotlarvaeorthoseobviouslydyingfrommaggotfeed-
spring;2)damagereductionswouldoccurbecauselater ing,butnolarvapresent,wererecordedasdeadand
plantingswouldescapeovipositionandelicitlessovipo- then removed from the plot. Periodically, maggots
sitionthanolder,largerplants;and3)inherentlygreater were randomly collected from seedlings, reared to
resistance of older plants to D. antiqua attack would adultandthenidentiÞedusingakeybyBrooks(1949)
lessen under high densities, explaining why a greater toensurethatmaggotsencounteredwereD.antiqua
resistanceofearly-plantedonionsdoesnottranslateinto andnotseedcornmaggot,Deliaplatura(Meigen).D.
reduced damage. Feasibility of a delayed planting to antiquawastheprimaryspeciesfound.
produceanonioncropthatyieldswellwasalsoinves- Onion seedlings may be killed by high winds and
tigated. seedlingdiseases,factorsthatconfounddataanalyses
examiningseedlingmortalityduetomaggotfeeding.
Therefore,datawereanalyzedinthefollowingman-
MaterialsandMethods
ner.First,thecumulativenumberofseedlingskilled
Planting Date and Maggot Damage in the Field. by maggots was determined through the end of the
Field experiments were conducted on muck soil in Þrstlarvalgeneration.Next,thistotalwasdividedby
commercial Þelds across the major onion producing thesumofallmaggot-killedplantsplustheÞnalplant
regionsofNewYork.Approximately40%oftheonions standcount,whichwastakeninmid-July.Thisquo-
1624 JOURNALOFECONOMICENTOMOLOGY Vol.104,no.5
tient was the Þnal proportion of plants killed by D. planted) in the model. Means were compared mid-
antiqua. These data were analyzed using a mixed season(n(cid:4)3)andatharvest(n(cid:4)2)usingLSMEANS
model(PROCMIXED),andtreatmentmeanswere at P (cid:2) 0.05. Data were not taken between July and
comparedusingLSMEANSatP(cid:2)0.05(SASInstitute harvestatthePineIslandsite.
2007). Treatment was considered as a categorical As in the 2003 experiment, female D. antiqua ßy
value(early,middle,orlateplanted)andaÞxedvari- activity was monitored at each site. Three yellow
ableinthemodel,whereasreplicationwasconsidered stickycardswerecollectedandreplacedonaweekly
random. Data were transformed using a square root basisbeginningattheestimatedstartoftheÞrstßight
(x(cid:3)0.001)functionbeforeanalysistostabilizevari- in May and continuing through the season as de-
ance,butuntransformedmeansarepresented. scribedpreviously.
ActivityofD.antiquafemaleswasmonitoredona 2005PlantingDateandCultivarExperiment. This
weekly basis beginning at the estimated start of the experimentwasconductednearPineIsland(Orange
Þrstßighton13May.Five(15by15-cm)yellowsticky County), Elba (Orleans County), Sodus (Wayne
cards(OlsonProducts,Medina,OH)wereclampedto County) and Oswego, NY (Oswego County). Culti-
stakesataninitialheightof13cmabovetheground. varsplantedwereMillennium,whichisalate-matur-
Thereafter,heightwasadjustedtokeepcardtopslevel ing,long-dayonion(110dafterplanting),andÔSher-
with the onion canopy. Cards were equally spaced manÕ,whichisanearly-maturing,long-dayonion(100
alongtheedgeofthetestsiteandreplacedweekly. d after planting). Seeds were planted as described
NumbersofD.antiquafemalesonbothsidesofeach previouslyineight-rowplotsthatwereeither9.1min
card were identiÞed following the key of Brooks length(Elba,SodusandOswego)or18.3minlength
(1949)andrecorded. (PineIsland),allatadensityof30seedsperm.There
2004 Planting Date Experiment. This experiment werethreeplantingdatesateachlocationandplant-
was conducted near Pine Island (Orange County), ingswerespacedapartapproximatelyevery2wk.In
Elba (Orleans County), and Sodus, NY (Wayne PineIsland,plantingswere14and29Apriland13May;
County). Millennium onion seeds were planted in inElba,plantingswere18Apriland4and16May;in
eight-rowplotsthatwereeither9.1minlength(Elba Sodusplantingswere15and29Apriland13May;in
andSodus)or18.3minlength(PineIsland),allata Oswego plantings were 6 and 20 May and 2 June.
density of 30 seeds per m. Seeds were planted as Treatments were randomly assigned within each lo-
describedinthe2003experiment.Therewerethree cation,buttreatmentswerenotreplicatedwithinsites.
planting dates at each location, and plantings were Locationwasconsideredthereplicate(n(cid:4)4).None
spacedapartapproximatelyevery2wk.InPineIsland, of the seeds were treated with insecticides, but all
plantings were 20 April and 5 and 19 May; in Elba, weretreatedwithPro-Groandsupplementedwitha
plantings were 29 April and 13 and 28 May; and in drench treatment of Dithane F-45 at the rates de-
Sodusplantingswere21Apriland4and17May.Half scribedpreviously.
of each plot was planted with seeds that were not PlantskilledordyingfromD.antiquawererecorded
treatedwithinsecticides,whereastheotherhalfwas asdescribedinthe2003experiment.Inaddition,50
plantedwithseedstreatedwithÞpronil(Regent6.2 bulbs were inspected for maggot damage approxi-
TS; BASF, Research Triangle Park, NC) at a rate of matelyevery2wkbeginning20July.Thepercentage
2.5g(AI)/100gofseedforprotectionagainstmaggots. ofbulbsdamagedoneachsamplingdatewasaddedto
AllseedsweretreatedwithPro-GroandDithaneF-45 themeancumulativepercentplantskilledbymaggots
asdescribedpreviously.Theexperimentwasasplit- earlierintheseason.Consequently,theresponsevari-
plot with planting date as the main plot factor and ablewasmeancumulativepercentageofplantskilled
insecticide-treatment as the subplot factor. Treat- andbulbsdamagedbymaggots.Thesedatawerean-
mentswerenotreplicatedwithinasiteandlocation alyzed using a mixed model (PROC MIXED), and
wasconsideredasthereplicate(n(cid:4)3). treatmentmeanswerecomparedusingLSMEANSat
PlantskilledordyingfromD.antiquawererecorded P(cid:2)0.05(SASInstitute2007).Plantingdate(categor-
asdescribedinthe2003experiment.Inaddition,atthe icalvalueasearly,middle,orlateplanted)andcultivar
Elba and Sodus sites, 50 bulbs were inspected for wereconsideredasÞxedvariables,whereaslocation
maggotdamageapproximatelyevery2wkbeginning wasconsideredrandom.Rawdataweretransformed
20 July. Because damaged bulbs are culled during usingasquarerootfunctionbeforeanalysistostabilize
grading, they were considered equivalent to a dead variance;backtransformedmeansarepresentedinthe
plant.Thepercentageofbulbsdamagedoneachsam- text.
plingdatewasaddedtothemeancumulativepercent TestInsectsforLaboratoryExperiments.D.antiqua
plantskilledbymaggotsearlierintheseason.Conse- eggs and ßies used in laboratory experiments de-
quently,theresponsevariablewasmeancumulative scribed below were obtained from colonies main-
percentage of plants killed and bulbs damaged by tainedinanenvironmentalchamber(21(cid:5)C,60%RH,
maggots.Datawereanalyzedasananalysisofvariance and a photoperiod of 16:8 [L:D] h) at Cornell Uni-
(ANOVA)forasplit-plotdesign(PROCGLM)(SAS versityÕsNewYorkStateAgriculturalExperimentSta-
Institute 2007). The replication by planting date in- tion in Geneva, NY. Colonies were established with
teractiontermwasusedasthemeansquareerrorfor larvaecollectedthepreviousyearfromonionÞeldsin
testingsigniÞcanceofplantingdate.Plantingdatewas YatesCounty,NY.Coloniesweremaintainedbypro-
given a categorical value (early, middle, or late vidingßiesadlibitumwithwaterandadietofbrewerÕs
October2011 NAULTETAL.:ONIONPLANTAGEIMPACTSONONIONMAGGOT 1625
yeast, powdered milk, sugar, and soy peptone Deadßieswerereplacedwithliveßies,andnewplants
(Ticheler 1971). Flies were allowed to oviposit in a wereplacedincagesforthesecondrun.
dish containing sand and a peeled onion; eggs then After the 48-h oviposition period, plants were re-
wereßoatedoutofthesandbyusingwater.Cohorts movedandthenumbersofeggsperpotcounted.Most
of similar-aged eggs were collected for experiments eggswerelaidwithinthetoponecmofsoilaroundthe
and for establishing subcolonies in which ßies of a baseoftheplantsandonlyafewwerelaidononion
certainagecouldbeobtainedforovipositionalexper- foliage.Themajorityofonionmaggoteggsaretypi-
imentsinthelaboratory. callylaidwithinthissoildepth(Havukkalaetal.1992).
Onion Plants for Laboratory Experiments. Mille- Soil was placed on a black surface, and eggs were
niumonionseedswereplantedinplastictraysÞlled sortedthroughwithapaintbrush.D.antiquaeggsare
with muck soil collected from a nearby commercial whiteandclearlyvisibleagainstablackbackground.
farm. All seeds received a Þlm-coating treatment of Datawereanalyzedusingapairedt-testimplemented
thiramandcarboxin(Pro-Gro)atarateof2.0g(AI)/ withPROCMEANSat(cid:2)(cid:4)0.05(SASInstitute2007).
100 g of seed to protect against seedling diseases. Short-DurationNo-ChoiceExperiment. Inthespring,
Plantswereallowedtogerminateinanenvironmental D. antiqua ßies typically emerge from the soil into
chamber (21(cid:5)C, 60% RH, and a photoperiod of 16:8 nonrotated, relatively large Þelds of onions. There-
[L:D] h) after which time they were transferred to fore,femalesprobablymakeovipositionaldecisionsin
pots(15.2by15.2cm)andmaintainedinthegreen- ano-choicesettingwhereplantsareallofrelatively
house (photoperiod of 16:8 [L:D] h) until plants similarage.Consequently,weusedno-choiceteststo
reachedthedesiredageforexperimentation. compareovipositionofD.antiquaon2-and8-wk-old
Ovipositional Experiments for Variously Aged plants.Plantsizetreatments,ßiesandcageswereob-
Plants. Choice and no-choice ovipositional experi- tained as described in the short-duration choice ex-
mentswereconductedinthelaboratorybyusingßies periment.Asingleplantfromoneoftheageclasses
andplantsasdescribedinthepreviouslysections.We mentioned above was randomly assigned to its own
were interested to know whether D. antiqua would cagecontaining207-d-oldD.antiquaßies,halfofeach
ovipositonlarger,olderonionplantsthanonyounger, sex.Eachtreatmentwasreplicatedthreetimes(n(cid:4)
smalleronionplantswheneithergivenachoiceornot 3), and there was a total of six cages. Flies were al-
givenachoicebetweenthetwotypesofplants.Based lowedtoovipositfor6d,afterwhichtimeplantswere
onresultssuggestingthatßiesmightwaittolayeggs removedandthenumbersofeggsperpotcountedas
untilplantsbecomelarger,asecondno-choicestudy described in the short-duration choice experiment.
wasconductedthatprovidedßiesamuchlongerpe- Few eggs hatched before 6 d; in the few instances
riod to lay eggs on young and old plants. A third wheneggsdidhatch,eitherlarvaeorchorionswere
no-choicestudywasconductedtocomparelevelsof counted.
damagetovariouslyagedonionplantswheninfested Thisexperimentwasrepeatedwiththesamecohort
withseveraldensitiesofD.antiquaeggs. ofplantsandßiesthatwereusedintheÞrstrun.The
Short-DurationChoiceExperiment. D.antiquaovi- second run was 1 wk later, so plant age treatments
positionalpreferenceforonionplantsvaryinginage werethen3and9wkoldandßieswere13dold.Cages
wasevaluatedinatwo-choicetestinthelaboratory. thatreceivedthetreatmentswererandomlychosenso
Onionseedswereplantedfourweeksaparttoobtain thatthesamecagedidnotalwaysreceiveplantsofthe
plantsthatwere3and7wkold.Sizesoftheseplants samerelativeageinthetworuns.Numbersofeggslaid
weresimilartothoseencounteredinalate(mid-to perpotwererecorded6dlater.Becausetherewasa
lateMay)andmid(lateApriltoearlyMay)planting one-wkagedifferencebetweenplantsandßiesused
of onions at the time ßies from the overwintering inthetworuns,datawereanalyzedseparatelyforeach
generation would be ovipositing. At this time, the run using ANOVA (PROC GLM), and means were
youngest plants had one to two leaves, whereas the comparedusingasingle-degree-of-freedomF-testat
olderplantshadthreetofourleaves.Theexperiment (cid:2)(cid:4)0.05(SASInstitute2007).
was conducted in a series of mesh cages (46 cm in Long-DurationNo-ChoiceExperiment. Resultsfrom
lengthby46cminwidthby46cminheight)thatwere the short-duration no-choice experiment suggested
keptinanenvironmentalchamber(21(cid:5)C,60%RH,and that D. antiqua adults might delay oviposition when
aphotoperiodof16:8[L:D]h).One3-wk-oldandone plantsareyoung,waitinguntiltheyareoldertode-
7-wk-oldplantwererandomlyassignedtoeachcage positeggs.Toaddressthispossibility,D.antiquaßies
andexposedtosevenfemaleandthreemaleD.antiqua wererestrictedtoonionplantsthatwereinitiallyei-
ßies.Flieswere7Ð10doldandwereofferedwaterand ther3or9wkoldandpermittedtoovipositonthese
thesamefoodprovidedtothecolonieswithincages. plantsuntiltheydied.Plantsizetreatments,ßiesand
Flieswereallowedtoovipositontreatmentplantsfor cageswereobtainedasdescribedpreviously;thestudy
48h.Tworunswereconducted,withsixreplicatesin wasconductedinthelaboratory.Asingleplantofeach
theÞrstandfourinthesecond,yieldingatotalof10 agewasrandomlyassignedtoitsowncagecontaining
replicates.Thesamecagesandßieswereusedforboth 10 female and 10 male D. antiqua ßies, all of which
runs;however,treatmentsandcageswerererandom- were7dold.Eachtreatmentwasreplicatedtentimes.
izedbeforethesecondrun.Therationaleforusingthe Plantswereremovedfromcagesafter1wk,andthe
sameßiesratherthannewßiesinthesecondrunwas numberofeggsperpotwascountedasdescribedin
becauseßieswerestillyoung(9Ð12dold)andfecund. short-durationchoiceexperiment.Plantswereimme-
1626 JOURNALOFECONOMICENTOMOLOGY Vol.104,no.5
Fig.1. MeancumulativepercentageofplantskilledbyÞrst-generationD.antiqualarvaethroughtime(solidline)inÞeld
plotsofonion(Millennium)plantedearly,mid,orlatespringinPotter,NY,in2003(n(cid:4)6).On15July,meansfollowedby
differentlettersindicateasigniÞcantdifference(P(cid:2)0.05;LSMEANS).MeannumberoffemaleD.antiquacapturedper
yellowstickycardperday(dashedline)atthetestsite(n(cid:4)5).
diatelyreplacedwithnewplantsfromthesamecohort weremadeonthesamedatesasintheplantingdate
(now 1 wk older), which were maintained in the Þeldexperiment.AllseedsweretreatedwithPro-Gro
greenhouse.Theexperimentwasconductedfor1mo, andsupplementedwithadrenchtreatmentofDithane
sotheagesofplantsinthetwotreatmentsattheend F-45attheratesdescribedpreviously.
ofthisexperimentwere7and13wkold.Totalnum- Marketableyieldwasdeterminedbyharvestingall
bersofeggslaidperpotoverthefoursamplingdates onionbulbswithinoneofthecenterrowsineachplot
for each treatment were analyzed using ANOVA in early to late August. Only marketable U.S. No. 1
(PROC GLM), and means were compared using a grade bulbs ((cid:6)3.8 cm in diameter) were harvested.
single-degree-of-freedomF-testatP(cid:2)0.05(SASIn- Data were analyzed using a mixed model (PROC
stitute2007). MIXED),andtreatmentmeanswerecomparedusing
PlantAgeandInsectDensityNo-ChoiceExperiment. LSMEANSatP(cid:2)0.05(SASInstitute2007).Planting
Thislaboratoryexperimenttestedwhetherolderon- date was considered as a Þxed variable, whereas lo-
ion plants were inherently more resilient against D. cationwasconsideredrandom.
antiqualarvaeacrossarangeoflarvaldensitiescom-
paredwithyoungerplants.Plantsizetreatments,ßies,
andcageswereobtainedasdescribedpreviously.One Results
differencefromtheotherlaboratoryexperimentswas
PlantingDateandMaggotDamageintheField
thatplantsweregrownin5.1-by5.1-cmpots.When
anonionplantwas2,4,6,or8wkold,itwasinfested 2003 Field Experiment. Fewer onion plants were
a single time with two, Þve, or 10 D. antiqua eggs. killedbymaggotsinplantingsmadelaterinthespring
Theseplantsweresubsequentlymaintainedinanen- (Fig.1).Onionsplantedinmid-Aprilweremorelikely
vironmentalchamberforthedurationoftheexperi- tobekilledthanthoseplantedineitherearlyorlate
ment(21(cid:5)C,60%RH,andaphotoperiodof16:8[L:D] May,whereasonionsplantedinearlyMayweremore
h). The experiment was a factorial and included all likelytobekilledthanthoseplantedinlateMay(F(cid:4)
combinations of seedling ages (four levels) and egg 42.0;df(cid:4)2,10;P(cid:2)0.0001).TheÞrstplantsinfested
densities (three levels). These treatments were ar- withmaggotsweredetectedon3,17,and24Junein
rangedinacompletelyrandomizeddesignreplicated early, mid, and late plantings, respectively (Fig. 1).
20times.After9d,eachplantwasrecordedaseither Fewonionplantswerekilledinalltreatmentsafter24
damagedbyD.antiquaornotdamaged.Plantswere June.D.antiquafemaleswereactivefrombeforemid-
considereddamagediftheyweredead,ßaccid,orfed MaythroughlateJuly,andtheiractivitypeakedon17
uponbylarvaebutnotßaccid.Thebinomialdatawere June. As a result, later plantings were exposed to a
analyzed using PROC GENMOD at P (cid:2) 0.05 (SAS much smaller portion of Þrst-generation ßies than
Institute2007).Datawererepresentedasthepercent- earlyplantings.Duringthisperiod,theearliestplanted
ageofplantsdamagedbyD.antiquaineachplantage onions had more leaves and were larger than those
byeggdensitycombination. plantedlater(B.A.N.,unpublisheddata).
Planting Date Impact on Bulb Yield Experiment. 2004FieldExperiment.Mid-SeasonEvaluation.De-
This experiment was conducted adjacent to each of layingplantingreducedD.antiquadamagetoonions
thefourlocationsdescribedinthe2005plantingdate (Figs. 2AÐC, and 3A). Onions planted in late April
Þeld experiment. Sherman onion seeds, protected ((cid:4)early)andearlyMay((cid:4)middle)weresigniÞcantly
with Þpronil seed treatment (Regent 6.2 TS) as de- morelikelytobekilledthanthoseplantedinlateMay
scribedinthe2004Þeldexperiment,wereplantedat ((cid:4)late)(F(cid:4)41.2;df(cid:4)2,4;P(cid:4)0.0021)(Fig.3A).
thesamedensitiesandinplotswiththesamedimen- Onionsgrownfrominsecticide-treatedseedweresig-
sions as described previously (n (cid:4) 4). All plantings niÞcantlylesslikelytobekilledcomparedwiththose
October2011 NAULTETAL.:ONIONPLANTAGEIMPACTSONONIONMAGGOT 1627
Fig.2. CumulativepercentageofplantskilledbyD.antiqualarvaethroughtime(solidlines)innoninsecticidetreated
Þeldplotsofonion(Millennium)plantedearly,mid,orlatespringinPineIsland,NY(A);Elba,NY(B);andSodus,NY(C),
in2004(n(cid:4)1ateachtestsite).MeannumberoffemaleD.antiquacapturedperyellowstickycardperday(dashedline)
(n(cid:4)3ateachtestsite).Notethatthescalesonthey-axesdifferamongsubÞgures.
nottreatedwithaninsecticide(F(cid:4)49.7;df(cid:4)1,6;P(cid:4) andwerelargerthanthoseplantedlater(B.A.N.,un-
0.0004)(Fig.3A).Onionskilledbymaggotswerenot publisheddata).
signiÞcantlyaffectedbyaplantingdatebyinsecticide Inmostplantingsatallsites,thepercentageofplants
treatmentinteraction(P(cid:6)0.05). killedbymaggotsdidnotincreasemuchbeyondearly
In Pine Island, plants infested with maggots were July.Onenotableexceptionwasthelateplantingin
Þrstdetectedon19Mayand8Juneinearlyandmid Elba(Fig.2B),whereanincreaseindamageinlate
plantings,respectively(Fig.2A).Nomaggotdamage July and August was caused by second-generation
wasobservedinthelatestplanting.InElba,maggots maggots.Inthiscase,late-plantedonionswereprob-
wereÞrstdetectedon7,13,and20Juneinearly,mid, ablyattractivetosecond-generationßiesandvulner-
and late plantings, respectively (Fig. 2B). In Sodus, abletoattackbymaggots.
maggots were Þrst detected on 1, 1, and 14 June in HarvestEvaluation. Resultsatharvestweresimilar
early,mid,andlateplantings,respectively(Fig.2C). tothoseduringmid-seasonbecausedamagetobulbs
D.antiquafemaleswereactiveinlateAprilandearly beyondmid-Julywasrelativelyminimalformosttreat-
Mayandpeakedonoraweekbeforemaggotswere ments(Fig.2BandC).OnionsplantedinlateApril
Þrstseenateachsite(Fig.2AÐC).Asinthe2003Þeld ((cid:4)early)weresigniÞcantlymorelikelytobekilledor
experiment,lateplantingsatallsiteswereexposedto tohavebulbsdamagedthanthoseplantedinlateMay
a much smaller portion of Þrst-generation ßies than ((cid:4)late)(F(cid:4)23.4;df(cid:4)2,4;P(cid:4)0.0409)(Fig.3B).
early plantings. During the time these females were Plantings in early May ((cid:4)middle) had similar num-
most active, earlier planted onions had more leaves bers of dead plants and bulbs damaged as the other
1628 JOURNALOFECONOMICENTOMOLOGY Vol.104,no.5
Fig.4. Meancumulativepercentageofplantskilledand
bulbsdamagedbyD.antiquaforanearly-maturing,long-day
onion(Sherman,100dfromplantingtoharvest)andalate-
maturing,long-dayonion(Millennium,110dfromplanting
toharvest),grownfromnoninsecticidetreatedseedplanted
early, mid, and late spring in New York in 2005 (n (cid:4) 4
locations).
Elba.Plantgrowthofbothcultivarsinthemidandlate
plantings in Oswego was much further behind the
Fig. 3. (A) Mean ((cid:7)SEM) cumulative percentage of
earlyplantingsbylateJulybecausetheywereplanted
plantskilledbyD.antiqualarvaeinthemiddleoftheseason
extraordinarily late (Fig. 5). These results indicate
ininsecticide-treatedornoninsecticidetreatedonions(Mil-
lennium) planted early, mid, or late spring 2004 (n (cid:4) 3 thatadelayinplantingbothearlyandlate-maturing
locations). (B) Mean ((cid:7)SEM) cumulative percentage of onioncultivarsbeyondmid-Maywillresultinsmaller
plantskilledplusbulbsdamagedbyD.antiqualarvaeinthe onions that have fewer leaves during the time Þrst-
sametreatmentsatharvest(n(cid:4)2locations).Meansfollowed generationßiesaresearchingforhosts.
bydifferentuppercaseletterssignifyasigniÞcantdifference
amongplantingdates,whereasmeansfollowedbydifferent
lowercase letters indicate signiÞcant differences between OvipositionalExperimentsforVariously
treatedanduntreatedonionswithineachplantingdate(P(cid:2) AgedPlants
0.05;LSMEANS).
Short-Duration Choice Experiment. Females laid
signiÞcantlymoreeggson7-wk-oldonionplantsthan
plantings (Fig. 3B). Onions grown from insecticide- on3-wk-oldplantswhengivenachoice(t(cid:4)2.39,df(cid:4)
treatedseedweresigniÞcantlylesslikelytobekilled 9,P(cid:4)0.0094).Nearlyfourtimesmoreeggswerelaid
or to have bulbs damaged compared with those not per7-wk-oldonionplant(37.6(cid:7)8.3)comparedwith
treatedwithaninsecticide(F(cid:4)81.7;df(cid:4)1,6;P(cid:4) a3-wk-oldonionplant(10.3(cid:7)3.6),indicatingthatD.
0.0029)(Fig.3B).Onionskilledanddamagedbymag- antiquaprefertolayeggsonolderplants.
gotswerenotsigniÞcantlyaffectedbyaplantingdate Short-Duration No-Choice Experiment. Females
byinsecticidetreatmentinteraction(P(cid:6)0.05). laidsigniÞcantlymoreeggson8-and9-wk-oldonion
2005FieldExperiment.Delayingplantingreduced plantsthanon2-and3-wk-oldonionswhenconÞned
D.antiquadamagetoplantsandbulbsforbothMil- totheseplantsfor6d(8-versus2-d-oldplants:F(cid:4)
lenniumandShermanonions(F(cid:4)40.1;df(cid:4)2,15;P(cid:2) 91.0;df(cid:4)1,4;P(cid:4)0.0007;9-versus3-d-oldplants:F(cid:4)
0.0001) (Fig. 4). Averaged across all planting dates, 14.1; df (cid:4) 1, 4; P (cid:4) 0.0199). No eggs were laid on
Shermanplantsweremorelikelytobekilledortohave 2-wk-oldplants,whereas30.3(cid:7)3.2eggswerelaidon
bulbsdamagedthanMillennium(F(cid:4)4.5;df(cid:4)1,15; 8-wk-oldplants.Lessthanathirdasmanyeggswere
P (cid:4) 0.05) (Fig. 4). Sherman plants grew larger and laidon3-wk-oldplants(45.6(cid:7)11.5)comparedwith
producedmoreleavesearlyintheseasoncompared 9-wk-old plants (167 (cid:7) 30.3). These results indicate
withMillenniumplants(datanotshown).Basedon thatifonionplantsaretooyoung,femaleswillnotlay
resultsfromourlabassaysthatindicatedanoviposi- eggsorwillnotlayasmanyastheywouldonlarger
tionpreferenceforlargeronionplants,ßiesmayhave plants.
beenmorelikelytoovipositonShermanthanMillen- Long-Duration No-Choice Experiment. Females
nium onions, and this would explain differences in laidsigniÞcantlymoreeggsonolderonionplantsthan
maggotdamage.Damagewasnotaffectedbyanin- onyoungeronionplantswhenconÞnedtotheseplants
teraction between cultivar and planting date (P (cid:6) foramonth(F(cid:4)16.3;df(cid:4)1,17;P(cid:4)0.0009)(Fig.6).
0.05). Females laid more eggs on older plants than on
Forbothcultivars,plantgrowthinthemidplantings youngerplantseachweekfor3wk,butnonewerelaid
caughtupquickly(lateJune)toplantgrowthinthe between3and4wk.Mosteggswerelaidwithin7din
earlyplantingsinSodusandElba(Fig.5).Incontrast, bothplantagetreatments,butthendeclinedsubstan-
plantgrowthinthelateplantingsdidnotcatchupto tially thereafter (Fig. 6). These results indicate that
theearlyplantingsuntilmid-tolateJulyinSodusand sexuallymaturefemaleswilllaymoreeggsononion
October2011 NAULTETAL.:ONIONPLANTAGEIMPACTSONONIONMAGGOT 1629
Fig.5. Proportionoftheheightandleavesperplantrelativetotheearliestplantedonionsateachofthreelocationsin
NewYorkin2005.Allearlyplantedonionshadaproportionof1.0.Sherman(100dtomaturity)andMillenniumonions(110
dtomaturity)wereplantedinearly,mid,orlatespring(n(cid:4)10plantsperobservation).
plantsifplantsareanappropriateageandsizewhen
Þrstencounteringthemcomparedwiththosethatare
too young and small. Females are not likely to wait
untilplantsgetolderandlargertolayeggs.
Plant Age and Insect Density No-Choice Experi-
ment.Plantageandeggdensityinteractedtoaffect
damageindifferentlyagedonionplants(Fig.7).Plant
damage was signiÞcantly affected by an interaction
betweenplantageandeggdensity((cid:3)2(cid:4)5.5,df(cid:4)1,
P(cid:4)0.0189)(Fig.7).Percentagesof2-and4-wk-old
onionplantswithmaggotdamagetendedtobehigh
regardless of egg density, whereas 6-wk-old onion
Fig.6. Mean((cid:7)SEM)numberofD.antiquaeggslaidper plantshadmoremaggotdamageatdensitiesofÞveto
plant each week for a month when restricted to onions 10 eggs per plant than at two eggs per plant, and
varying in age (n (cid:4) 3 for each treatment). Plants were 8-wk-oldplantshadmoredamageatadensityof10
initially3or9wkoldwhenplacedingroupsoffourincages eggsperplantthanattheotherdensities.Theseresults
thatinitiallycontained2010-d-oldßies(10ofeachsex)inthe
indicatethatasonionplantsgetolder,theybecome
laboratory. Eggs were counted, and plants were replaced
moreresilienttoattackbyD.antiqualarvaebutthat
eachweek.Meantotalnumberofeggsperplantwithdif-
ferent letters indicate a signiÞcant difference (P (cid:2) 0.05; thisresiliencybreaksdownunderhighmaggotden-
LSMEANS). sities.
1630 JOURNALOFECONOMICENTOMOLOGY Vol.104,no.5
likely to be attractive to ovipositing ßies. However,
these plants grew for 4 wk and were certainly large
enoughtobeattractivetoovipositingßies.Yet,few
eggswerelaid.Resultsfrompastresearchhaveshown
thatthereisadeterministicsequenceofpostalighting
oviposition behaviors required for D. antiqua to lay
eggsononionplants(Mowryetal.1989).Basedonour
results,onionplantsdidnotgrowquicklyenoughto
reachasizenecessaryforthepreovipositingbehaviors
toengageandforßiestolaymanyeggs.
OnionplantsbecamemoreresilienttoattackbyD.
antiqualarvaeastheyaged,butthisresiliencybroke
down under high maggot densities. Finch et al.
Fig.7. MeanpercentageofonionplantsdamagedbyD.
(1986a)conductedagreenhouseexperimenttomea-
antiquaafter1wkofexposuretotreatmentsthatvariedin
sure the effects of onion plant age on D. antiqua
plantageandinfestationdensitiesinthelaboratory.
survivaltopupation.Onionplantswerecollectedfrom
theÞeldinNewYorkon19Julyand10and24August,
PlantingDateImpactonBulbYieldExperiment
andeachplantwasinfestedwith40eggs.Thirty-seven
Marketable bulb yield did not differ signiÞcantly percentofD.antiquaeggssurvivedtopupationwhen
amongplantingsofShermanonions(P(cid:6)0.05).Bulb fed plants collected on 19 July, whereas 1.6 and 0%
yieldwas51.7(cid:7)5.7,47.7(cid:7)10.4,and43.4(cid:7)8.5T/ha survivedtopupationontheolderplants.Theycon-
forearly,mid,andlateplantings,respectively.These cludedthatbulbsbecomeinherentlymoreresistantto
resultsindicatethatplantinganearly-maturing,long- penetration by D. antiqua as onions mature. In our
dayonionlateintheseasontoreducemaggotdamage study, plants were much younger (e.g., prebulbing
shouldproduceamarketableonioncrop. stages)thantheplantsusedintheFinchetal.(1986a)
study.Despitethisdifference,weobservedthesame
results:olderplantshadlessdamagebymaggotsthan
Discussion
youngerplants.Wealsofoundthatolderonionplants
D.antiquadamagetoplantsandbulbswasconsis- becamelessimpervioustomaggotdamageasmaggot
tently lower in later plantings of onions. Onions densitiesincreased.Plantsthatwere6-to8-wkoldhad
plantedlateremergedlaterandthisreducedthepe- (cid:8)2.5timesmoredamagewheninfestedwith10eggs
riod that overwintered ßies had to oviposit on the comparedwithtwoeggs.
plants.Moreover,ßiestendedtolayfewtonoeggson AdelayinonionplantingreducedD.antiquadam-
these young, late-planted onions. This suggests that age. Based on results from our Þeld experiments
plantingonionslaterinthespringreducesdamageby (2003Ð2005),numbersofonionplantskilledorbulbs
allowingplantsto“escapeintime”andbytakingad- damagedbyD.antiquawerereducedonaverageby35
vantageofD.antiquaovipositionalbehavior.Wealso and90%whenonionswereplanted2Ð3wkand4Ð6wk
discoveredthatresistanceofolderplantstoD.antiqua laterthantheearliestplantedonionsinthatregion,
larvaebrokedownunderhighdensities.ThisÞnding respectively. A delay in planting 2Ð3 wk after the
suggeststhatduringtheÞrstgenerationanybeneÞts earliestplanting,whichtypicallyoccurredbetween29
ofincreasedresistanceinolderplantingswillbeoffset Aprilto20May((cid:4)midplantingdatetreatment),did
by increased egg densities, explaining why greater not reduce damage to an acceptable level (mean (cid:4)
maggotdamagewasobservedinearlyonionplantings 24%).Incontrast,planting4Ð6wkaftertheearliest
comparedwithlaterplantings. planting, which typically occurred between 13 May
D.antiqualaidmoreeggsonolderonionplantsthan and 2 June ((cid:4)late planting date treatment), did re-
onyoungplants,regardlessofwhetherßiesweregiven ducedamagetoanacceptablelevel(mean(cid:4)4%).A
a choice between the two age categories of plants. delayinplantingbyonly2Ð3wkwouldnotbeastand
Whengivenachoice,ßieslaid4timesmoreeggson alone management tactic for D. antiqua, whereas it
olderplantsthanonyoungplants.Whenßieswerenot couldbeforonionsplanted4Ð6wklaterthannormal.
givenachoice,ßieslaidfourto7timesmoreeggson ThereductionindamagecausedbyD.antiquain
older plants. Moreover, when ßies were exposed to Þeldsplantedlaterintheseasonwasprobablydueto
onionsforamonthbeginningwhenplantswereyoung temporalasynchronybetweenfemaleßiesandonion
andsmall,ßieslaidfewereggscomparedwiththose plants of sufÞcient size to elicit oviposition. Later
that were initially offered older and larger plants. plantingsofonionsescapedintimefromtheperiod
Theseresultssuggestthatovipositioncuesareelicited femalesweremostactiveandlikelyovipositing(Figs.
when ßies are young. Harris et al. (1987) demon- 1and2),andtheseplantsweresmallandunlikelyto
stratedthatD.antiquaovipositionincreasedwithan beattractivetoovipositingßies(Fig.7).Plantingon-
increase in onion stem diameter and may likewise ions in late May to early June in New York rarely
explainwhyD.antiqualaidmoreeggsonlargerplants, occurs because it constitutes an economic risk to
whichhappenedtobeolderandplantedearlier.Inour growers.OniongrowersusuallyplantÞeldsasearlyas
long-durationno-choiceexperiment,weconÞnedßies soil moisture conditions permit to maximize the
tocagescontainingsmallonionplantsthatwereun- amountoftimeavailableforplantstoproducefoliage