The role of two eulophid parasitoids in populations of the leafminer, Phyllonorycter mespilella (Lepidoptera:Gracillariidae) in British Columbia

8 Pages·1994·4.4 MB·English

by  J E Cossentine

J.Entomol.Soc.Brjt.Columbia91,December, 1994 47
The role oftwo eulophid parasitoids in populations
ofthe leafminer,Phyllonoryctermespilella
(Lepidoptera:Gracillariidae) in British Columbia
J.E. COSSENTINEand L.B.JENSEN
AGRICULTUREANDAGRI-FOODCANADA,RESEARCHCENTRE
SUMMERLAND,BRITISHCOLUMBIA,CANADAVOH1ZO
CONTRIBUTIONNO.894
ABSTRACT
In 1991, orchards in the Naramata region ofthe Okanagan valley in British Columbia had
significantly largerpopulations ofthe leafminer,Phyllonoryctermespilella, than those ofthe
Osoyoos/Oliverregion,50kmsouth,whereparasitismhadbeenshowntokeeptheminerbe-
lowtreatmentlevels.Wequestionedifdifferentrolesoftheparasitoidspeciescausedthedis-
crepancy. Leaves werecollectedand leafminers andparasitoidsassessed from overwintering
populationsandalsoweeklyfromMaythroughOctober(1992) in appleorchardsrepresenta-
tive ofthe areas. Pnigalioflavipes and Sympiesis marylandensis were the major parasitoid
speciesoverwinteringin52.3and46.7%respectivelyoftheP.mespilellamines.Thepercent-
agesofthetwospeciesdidnotdiffersignificantlybetweentheorchardsscreenedinbothareas
anddidnotaccountforthedifferencesinthenumbersofoverwinteringorsummergeneration
mines.P.flavipeswasthedominantparasitoidspeciesinbothregionsthroughthethreesummer
generations.5.marylandensiswasonlyfoundatlowlevelsinthreeoftheeightorchardsuntil
thesecondandthirdgenerations.Parasitoid-induced-mortalityin 1992didnothaveaconsistent
significant impact on intraseasonal leafminer increase. Five of the orchards studied had
leafminerpopulationsabovetreatmentthresholds.
Keywords:Treefruit,biologicalcontrol,Hymenoptera,leafminer
INTRODUCTION
Phyllonoryctermespilella{=elmaella)(Hubner)(Lepidopera: Gracillariidae),isatentiform
leafminerthatfeedswithintheleavesofseveraleconomicallyimportantfruittreesinthePacific
Northwest(Hoyt 1983).Fourparasitoidspecieswereassociatedwiththisleafminerwhenitwas
firstestablishedintheorchardsoftheOkanaganandSimilkameenvalleysofBritishColumbia
in 1988 (Cossentine andJensen 1992). Pnigalioflavipes (Ashmead) (Hymenoptera: Eulophi-
dae)wasidentifiedasthemajorparasitoidoftheleafminerinBritishColumbianandWashing-
tonStateorchards(Barrett 1988,CossentineandJensen 1992).Parasitismbythisspeciescould
reducethehost'sintraseasonalpopulationincreaseandkeepitsdensitybelowtreatmentlevels
(BarrettandBrunner1990).Thevalueoftheotherthreeleafminerparasitoids,speciesofSymp-
iesis, Eulophus and Cirrospilus (Hymenoptera: Eulophidae), incontrol ofP. mespilella inthe
interiorofBritishColumbiahavenotbeenstudied.
Inthe 1991 applegrowingseason,orchardsintheNaramataareaoftheOkanaganvalleyhad
veryhighpopulationsofthe leafminer. Thiswas incontrasttothe well controlledpopulations
ofP.mespilellaintheOsoyoosandOliverorchards,about50kmfurthersouthwherePflavipes
was first established, and its effective role in regulating the leafminerpopulations during the
summerbecameevident(CossentineandJensen 1992). Inthe 1992growingseasonwesought
todetermine ifthe parasitoids and theirroles differed between the twoareas, and ifthese dif-
ferencescouldexplainthevariationintheleafminerpopulations.
MATERIALSAND METHODS
In 1992 we selected five orchards in the Naramata area that had high populations ofP.
mespilella in 1991 and three in the Oliver/Osoyoos area which had low populations thathad
beenwellcontrolledbyparasitisminthepast.MoreorchardsandleaveswerescreenedinNara-
48 J.Entomol.Soc.Brit.Columbia91,December, 1994
mata,becausejudgingfromhighleafminercounts inpreviousyears,weexpectedfewerpara-
sitoidswouldbefound.
WecollectedleavesinJanuary 1992(Naramata200,Oliver/Osoyoos 100)fromtheorchard
floorateachsitebeforewinterdiapauseoftheleafminerorparasitoidpupaewasbroken.Leaves
fromeach orchard were placed inaventilated 2-1plastic containerandheldatroomtempera-
ture(20-22°C).Thecontainerswerecheckeddailyforparasitoidemergenceandtheadultpar-
asitoidswerefrozenuntilidentifiedandsexed.Representativespecimenswereidentifiedbysys-
tematists atthe Centre forLand and Biological ResourcesResearch,Ottawa. Comparisonsof
emerging parasitoids were based on the assumption that each species would have an equal
chance ofsuccessfully developing under the described conditions. The leaves from three or-
chards in Naramata were so severely torn that mines perleafcould notbe assessed. Anesti-
mated appropriate massoftornleaves was therefore collectedfromeachofthese orchards so
thatemergingparasitoidadultscouldbecollectedandidentified.
Onehundredleaveswerecollectedrandomlyfromthecanopyofeachorchardweeklyfrom
May7untilOctober5,andonOctober24.Theinfestationlevelwasdeterminedbycountingthe
minesperleafandassessingtheminecontentsoftheseleaves.Thiscountincludedthenumbers
oflivinganddeadsap-feeders(instars 1-3)andtissue-feeders(instars4-5),pupae,emergedpu-
pae,parasitoideggs,larvaeandpupae,mineswitharoundparasitoidexithole,aswellasempty
mines. Leaves containing parasitoids in any stage ofdevelopment were placed in ventilated
2-1plasticcontainersandtheemergingparasitoidadults were aspirated,frozenandlateriden-
tifiedandsexed.
PnigalioandSympiesisspp. causeleafminermortalitybothaslarvae whichfeedexternally
onhost larvae as well as adults 'host-feeding' onleafminerlarvae andoccasionally onpupae
(Barrett 1988, Van Driesche and Taub 1983). In the first generadon total parasitoid-induced-
mortality (PIM) wasassessedasthenumberofminescontainingdeadleafminersand/orpara-
sitoidsdividedbythetotalnumberofminesminusthenumberofemptymines.Thefateofthe
P.mespilellafromemptyminescouldnotbedetermined.Inthesecondandthirdgenerationsthe
PIMandtotalnumberofminesperleafwereassessedasabove;however,mineswithemerged
pupae,emptyminesandparasitoidexitholeswereremovedfromthecalculadonsbecausethey
mayhaveoccurredinthefirstgeneration.Thenumberofparasitoidsemergingperminewasde-
Table1
Phyllonoryctermespilellaminesperoverwinteredappleleafandforeachsummergeneration,assessedon
100leavesatpeaksap-andtissue-feedingstages.
Minesperappleleaf
Overwintering FirstGeneration SecondGeneration ThirdGeneration
(n) sap tissue sap tissue sap tissue
NaramataOrchards
1. 11.00(200) 0.07 0.06 1.07 1.84 4.82 7.48
2. 5.57(200) 0.36 0.03 1.88 3.55 5.32 5.78
3. 0.03 0.02 0.41 1.79 6.82 7.53
4. 0.00 0.00 0.08 1.03 2.46 6.54b
5. 0.19 0.15 2.02 4.18 9.33 13.94
Osoyoos/OliverOrchards
1. 2.76(100) 0.10 0.06 2.71 4.25 14.64 15.64
2. 0.44(100) 0.02 0.02 0.24 0.58 2.90 2.82
3. 1.22(100) 0.02 0.01 0.75 1.76 7.63 8.10
leavesweretornandminesperleafcouldnotbedetermined,
'countfrompreviousweek,orchardcutdown.
' '
J.Entomol.Soc.Brit.Columbia91,December, 1994 49
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50 J.Entomol.Soc.Brit.Columbia91,December, 1994
Table3
Mortality attributed to parasitoids (PIM) per 100 apple leaves at peak tissue-feeding Phyllonorycter
mespilellastageswithineachofthreesummergenerations.
Mortality^
FirstGeneration SecondGeneration ThirdGeneration
NaramataOrchards
1. 38.6b 87.9 96.8
2. 32.9 72.7 100.0
3. 8.2 47.0 99.2
4. 50.0 34.4 79.5
5. 75.8 86.7 99.5
Osoyoos/OliverOrchards
1. 19.7 95.3 87.0
2. 42.0 84.2 94.6
3. 30.2 80.5 99.3
Mortalitywasconsideredtoinclude:parasitoideggs,larvae,pupae,parasitoidexitholes(firstgeneration
only)anddeadhostlarvaeandpupaedividedbytotalmines(excludingminescontainingemplypupae,
parasitoidexitholesoremptyminesinthesecondandthirdgenerations),
''eachvalueinthetablerepresentstheassessmentper 100mines.
teirnined as the total ofadultparasitoids divided by the numberofminesperleafassessed as
above.
Parasitoid and leafminercounts were not averaged overweeks withingenerations because
eachsamplecouldnotbeconsideredareplicateofanextendedstabilizedpointinthehost-par-
asitoidlifehistories(VanDriesche 1983).Rather,theleafminerpopulationswerecomparedat
fiveindividualweeksduringmaximumsap-feedingandtissue-feedingstageswithineachgen-
eration. PIM wasassessedatthepeaktissue-feeding stage whenconditions were mostoppor-
tuneforparasitismandhost-feeding.
P. mespilellaminesperleaf,parasitoidspermineandPEM werecomparedbetweenthetwo
regionsusingan ANOVA(SAS Institute 1985).Percentparasitism,thesexofeachparasitoid,
minesperleafand PIM within the overwinteringpopulation werecomparedbetweenthetwo
regionsusingacorrelationprocedure (SASInstitute 1985).
RESULTS ANDDISCUSSION
Overwinteringpopulation.LeavescollectedinJanuaryfromorchardsintheNaramataarea
contained significantly (p=0.04) higher numbers ofmines per leafthan did leaves collected
from OliverandOsoyoos orchards (Table 1). This illustrates thecontrasting infestationlevels
betweenthe twoorcharding regionsobserved in 1991. Emerging total numberofoverwinter-
ingparasitoidsperminedidnotdiffersignificantly(p>0.05)betweenthetworegions(Table2).
P.flavipesandSympiesismarylandensisGirault(Hymenoptera:Eulophidae)(identifiedbyJ.
Huber,CentreforLandandBiologicalResourcesResearch,Ottawa)weretheparasitoidspecies
mostcommonlyreared from overwinteringP. mespilellamines. S. marylandensisisprobably
thesamespeciesofSympiesispreviouslyrecordedasaminorparasitoidoftheleafminerinthe
Okanagan valley (Cossentine and Jensen 1992), although it is not one ofthe three species of
Sympiesis previously cited as parasitizing Phyllonorycter elmaella in the Eraser valley (Do-
ganlarandBieme 1980).
P.flavipes represented 52.3% and S. marylandensis 46.7% ofthe overwintering parasitoid
populationsintheeightorchards(n=358).ThiswasunexpectedasP.flavipeswasthedominant
parasitoidspeciesinthe summerstudiesof1988-1990(Cossentine andJensen 1992) andwas
thereforeexpectedto infestahigherproportionoftheoverwinteringmines. Percentageofthe
1
J.Entomol.Soc.Brit.Columbia91,December, 1994 51
totalpopulationvariedfrom0to 85.7% andfrom 14.3 to 100% forP.flavipesand S. marylan-
densis, respectively. The percentages ofP.flavipes and S. marylandensis in the overwintering
mines did not differ significantly (/?>0.05) between the two regions. Barrett and Jorgensen
(1986)reportedthatS. marylandensiswasthedominantparasitoidspeciesofthefirstandthird
P. elmaellagenerationsinUtahandthatPflavipeswasdominantinthesecondandfourthgen-
eradons.Thepercentagesofmaleandfemaleadultsofeachofthetwoparasitoidspeciesdidnot
differ significantly (p>0.05) between the two regions (Pnigalio male:78.5%, 61.9%; female:
21.5%,38.2%; Sympiesismale: 78.7%,90.5%;female: 21.3%,9.5%, intheNaramataandOs-
oyoos/Oliverregions,respectively).
Zagrammosomamultilineatum(Ashmead) (Hymenoptera:Eulophidae), aspeciesnotprevi-
ouslyrecordedfromP. mespilellainBritishColumbia(CossentineandJensen 1992,Doganlar
andBieme 1980)represented6.06%oftheparasitoidpopulationemergingfromoneNaramata
1 1 1 1
A. Mines/leaf 0.30
J
Naramata -o- P.f/av/pos/mine
12.0 .
||
II S.marylandens/s/mine
1
1 « n 0.20
9.0 « « }
~ •"
6.0
0.10
U. 3.0
<
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0.0 0.00
CO
LU ^- /\ 0.30
Osoyoos
12.0 ^ ]
V:
0.20
9.0
6.0
0.10
3.0
0.0 0.00
May 27 July 2 Aug 5 Sept 9
DATE
Figure1. PhyllonorycterminesperleafandparasitismbyPnigalioandSympiesisperminefromMayto
October 1992.A=orchard 1,Naramata;B=orchard 1,Osoyoos/Oliver.
52 J.Entomol.Soc.Brit.Columbia91,December, 1994
orchard. Over all orchards this represented only 0.76% (n=385) of the overwintering para-
sitoids.
Summerpopulations.Thenumberofsapfeedingminesperleafdidnotdiffersignificantly
(/?>0.05) between the two regions in the first generation (Naramata: x=0.13 mines/leaf,
Oliver/Osoyoos: x=0.05mines/leaf)(Table 1).Wethenquesdonedifthepercentparasitismby
each species independently,orthe sexrafioofP.flavipesorS. marylandensiswithintheover-
winteringpopulation, affectedthenumberofP. mespilellaminesperleaforpercentofPIMin
the firstgeneration. None ofthesefactors inthe overwintering populationconsistently orsig-
nificantly (p>0.05) influencedmines perleaforPIM in the firstgenerationwhencounts were
analyzed as separate regions and as a whole (Tables 1 and 3). The number ofoverwintering
mines wasnot significantly correlatedwiththe numberofsap-feeding (r=0.2,/?=0.63)) ortis-
sue-feeding (/-=0.65,/?=0.23) mines inthe firstgeneration. This contradicts BarrettandBrun-
ner's(1990)conclusionthatthe survival ofoverwinteringleafminers,ratherthantheseasonal
levelsofparasitism,determinetheleafminers' year-to-yearpopulationdynamics.
May 27 July 2 Aug 5 Sept 9
DATE
Figure2. Proportionineachdevelopmentalstage:A=parasitoidsPnigalioandSympiesis;B=leafminer
Phyllonorycterd&itnnmtd.fromweeklysamplesMaytoOctober 1992fromorchard 1,Naramata.
J.Entomol.Soc.Brit.Columbia91,December, 1994 53
Throughoutbothregions,Rflavipesremainedthedominantparasitoidspeciesoverthethree
generations. Significantly (p<0.05)moreRflavipesemergedper 100minesthandidanyother
parasitoid species in all three generations. Despite its majorrole in the overwintering popula-
tions, S. marylandensisrepresented a small percentofthe parasitoids inthe firstsummergen-
eration(Table2,Fig. 1), increasing in itsrole asaparasitoid inthe secondgeneration.
Themeannumberofminesperleafdidnotdiffersignificantly(p>0.05)betweenthetwore-
gions inthesecondgeneration(Table 1). Mortalitycausedbyhost-piercingandovipositionof
RflavipesandS. marylandensisinthefirstgenerationwasexpectedtobenegativelycorrelated
withthenumberofminesperleaffoundinthesecondandthirdgenerations(BarrettandBrun-
ner1990,CossentineandJensen 1992,VanDriescheandTaub 1983).Thiswastrueonlyforthe
Osoyoos/OliverregionwherethePIMinthetissue-feedingstageofthefirstgeneradonwassig-
nificantlynegativelycorrelated(r=0.90-0.96,/?<0.05)withtheminesperleafinthesecondgen-
eradonoveratwo-weekperiod.
The economic treatment threshold for leafminers in apple has been estimated at one sap-
feederperleafforthe first generation, two sap-feeders perleafforthe second generationpro-
videdthatPIM is<30% inthe firstgeneration,and five sap-feeding minesperleafinthe third
generation (Hoyt 1987). The only orchard sampled in this study thatexceeded this treatment
thresholdinthe secondgenerationwasintheOhver/Osoyoosregion.Leafminercounts inthis
orcharddid notexceedthresholds in 1991. Despite finding six ofthe eightorchards with PIM
above30%inthefirstgeneration(Table3),fiveoftheeightorchardshadexceededthetreatment
thresholdbythethirdgeneration(Table 1).
Toexplainthehigh 1992P. mespilellapopuladons,thewarmweatherearly inthe season in
1992 may have allowed the leafminers to establish large populations before Rflavipes could
haveasignificantcontrollingeffect.Unfortunately,neitheremergenceofadultRmespilellanor
theparasitoidspecieswasassessedinthespringtojudgeiftheiremergencesweresynchronized.
In Connecticut, adult S. marylandensis emerged two to four weeks before its host, Rhyllono-
rycterblancardella, inthe spring (Maier 1984). 5". marylandensis, which made upabout50%
oftheoverwinteringparasitoidpopulation,didnotappeartoinfluenceP.mespilellacontrolun-
tilthesecondandthirdgenerationsbywhichtimetheleafminerpopulationswerealreadyabove
economic thresholds in someorchards. Thedevelopmental stages oftheparasitoids appearto
be in synchrony with those ofthe leafminerhost in the firsttwo summergeneradons (Fig. 2),
withtheparasitoidspupatingjustattheendofthe R. mespilella'^firstgenerationandthepara-
sitoideggsbeing laid atthebeginningofgenerations twoandthree. Theparasitoidsappearto
havetwogenerationsduringthe leafminersthird(Fig. 2).
Parasitoid-induced-mortality increased withgeneration (Table 3),contrary towhatwas ob-
servedbyBarrettandBrunner(1990)buttheyexcludedminesjudgedtobefromanearliergen-
eradonintheircounts. Weexcludedminesbutthatwereemptyorcontained anemergedpupa
oraparasitoidhole.Wedonotbelievethatthedeadlarvaecouldbeassignedtoaparticulargen-
erationconsistendy.ThehighPIMinthesecondandthirdgenerationsinourstudymaybepar-
tially due tothe accumuladon ofdead larvae from previous generations. Howeverthe PIM in
the second and third generations was also high when compared to studies done in a similar
fashion inthe Okanaganvalley from 1988 to 1990 (Cossentine andJensen 1992). These high
percentagesindicatethatalownumberofliveleafminerswouldbefoundinthe 1992-93over-
winteringmines.Thismust,atleastinpart,accountforthelowpopulationsofR.mespilellaob-
servedinthesummerof 1993.
We conclude that the percentage ofP.flavipes and S. marylandensis in the overwintering
leafminerpopulationof1991-92didnotdifferbetweentheorchardsscreenedinNaramataand
Oliver/Osoyoos,andcouldnotexplain thedifferences in the numberoffirstgenerationmines
inanyoftheeightorchards.WefoundR.flavipestobethedominantparasitoidinthethreesum-
mergeneradons.S.marylandensisdidnotstarttoparticipatewithinthecomplex,exceptatlow
levelsinthreeorchards,untilthesecondgeneration.NeithertheEulophusorCirrospilusspecies
previously foundparasidzing the leafminerinthe south OkanaganvalleyofBritishColumbia
werefoundintheorchardsstudied.
Theleafminerparasitoidcomplexisusuallyanefficientandeffectivebiologicalcontrolofthe
54 J.Entomol.Soc.Brit.Columbia91,December, 1994
hostpopulations. In 1992leafminersexceededeconomic thresholds inorchards intheOkana-
ganvalley. NeitherP.flavipesorS. marylandensishadasignificantinfluenceon intraseasonal
leafminerincrease. However, increasing season-longPIMhadadramatic impactonthenum-
berofleafminersenteringoverwinteringdiapauseinthefallof 1992.
ACKNOWLEDGEMENTS
We thankDebbieBensenforhertechnical assistance and Mark Gardinerforpreparing the
graphs.
REFERENCES
Barrett,B.A. 1988.ThepopulationdynamicsofPnigalioflavipes(Hymenoptera:Eulophidae),themajorparasitoidof
Phyllunorycterelmaella (Lepidoptera: Gracillariidae) incentralWashingtonappleorchards. Ph.D.dissertation,
WashingtonStateUniversity,Pullman.
Barrett,B.A.andJ.F.Brunner. 1990.TemporaldistributionofPhyllonorycterelmaella(Lepidoptera:Gracillariidae)and
itsmajorparasitoidPnigalioflavipes(Hymenoptera:Eulophidae),inWashingtonappleorchards.Environ.Ento-
mol. 19(2):362-369.
Barrett;B.A.andCD.Jorgensen. 1986.ParasitoidsofthewesterntentiformleafminerPhyllonorycterelmaella{Lep-
idoptera:Gracillariidae),inUtahappleorchards.Environ.Entomol. 15:635-641.
Cossentine,J.E.andL.B.Jensen. 1992.EstablishmentofPhyllonoryctermespilella(Hubner)(Lepidoptera:Gracillari-
idae)anditsparasitoid,Pnigalioflavipes(Hymenoptera:Eulophidae),infruitorchardsintheOkanaganandSim-
ilkameenvalleysofBritishColumbia.J.Entomol.Soc.Brit.Columbia.89:18-24.
Doganlar,M.andB.Bieme. 1980.ParasitesofPhyllonorycterelmaella(Lep.:Gracilariidae)onappleintheVancou-
verdistrict,BritishColumbia.Can.Entomol. 112:314.
WA
Hoyt,S. 1983.Biologyandcontrolofthewesterntentiformleafminer.Proc. Hort.Assoc.79:115-118.
Hoyt,S.C.1987.Impactandthresholdsoftheleafmineronapple,pp.7-9.In:Leafminershortcourse.WashingtonState
University,CollegeofAgricultureandHomeEconomics,CooperativeExtensionService. 17p.
Maier.C.T. 1984.Abundanceandphenologyofparasitoidsofthespottedtentiformleafminer,Phyllonorycterblan-
cardella(Lepidoptera:Gracillariidae),inConnecticut.Can.Entomol. 116:443-449.
SASInstitute. 1985.SASUser'sGuide:Statistics,Version5edition.SASInstitute,Gary,N.C.956pp.
Van Driesche, R. G. 1983. Meaning of"Percent Parasitism" in studies of insect parasitoids. Environ. Entomol.
12(6):1611-1622.
VanDriesche,R.G.andG.Taub. 1983.ImpactofparasitoidsonPhyllonorycterleafminersinfestingapplesinMassa-
chusetts,U.S.A.Prot.Ecol.5:303-317.