Parasitoid Guild and Parasitism Rate of the Obliquebanded

Document généré le 30 sept. 2021 05:34

Phytoprotection

Parasitoid guild and parasitism rate of the obliquebanded leafroller in IPM orchards and adjacent woodlands Guilde de parasitoïdes et taux de parasitisme de la tordeuse à bandes obliques dans les vergers de pommiers sous lutte intégrée et dans des boisés adjacents Jacinthe Tremblay, Paula Cabrera, Daniel Cormier, Jacques Brodeur et Éric Lucas

Volume 98, numéro 1, 2018 Résumé de l'article Choristoneura rosaceana (Harris) [Lepidoptera : Tortricidae] (TBO), ravageur URI : https://id.erudit.org/iderudit/1055354ar primaire des vergers de pommiers au Québec, peut être naturellement DOI : https://doi.org/10.7202/1055354ar parasitée. Étant donné que les habitats près des périphéries des cultures sont des réservoirs pour les ennemis naturels des ravageurs, l’objectif de cette Aller au sommaire du numéro recherche était d’évaluer le parasitisme et la diversité des parasitoïdes de la TBO. L’étude sur deux ans porte sur les vergers sous régie intégrée, leurs lisières et boisés adjacents. Le parasitisme fut évalué avec des larves Éditeur(s) sentinelles de TBO, placées à différentes périodes (printemps, début, fin d’été). L’année 1, seules les larves de fin d’été ont présenté des différences Société de protection des plantes du Québec (SPPQ) significatives entre les zones : parasitisme supérieur en verger (27 %), comparativement à la lisière (7 %) et aux boisés (11 %). L’année suivante, les ISSN larves exposées en début d’été présentaient un parasitisme supérieur en lisière (28 %), par rapport aux larves en verger et dans les boisés (17 %). Dix-neuf 1710-1603 (numérique) espèces de parasitoïdes ont attaqué les larves sentinelles de TBO. Le tachinaire Actia interrupta (Curran) était le plus abondant (28 % année 1 et 62 % année 2). Découvrir la revue Nos résultats démontrent que la régulation naturelle de la TBO est le résultat de l’action d’une guilde très diversifiée de parasitoïdes, qui doit être prise en compte dans tout programme de lutte. Citer cet article Tremblay, J., Cabrera, P., Cormier, D., Brodeur, J. & Lucas, É. (2018). Parasitoid guild and parasitism rate of the obliquebanded leafroller in IPM orchards and adjacent woodlands. Phytoprotection, 98(1), 36–45. https://doi.org/10.7202/1055354ar

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Parasitoid guild and parasitism rate of the obliquebanded leafroller in IPM orchards and adjacent woodlands

Jacinthe Tremblay1, Paula Cabrera2, Daniel Cormier3, Jacques Brodeur4 and Éric Lucas5

Received 2018-05-23; accepted 2018-07-01

PHYTOPROTECTION 98 : 36-45

The obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris) [Lepidoptera: Tortricidae], a pri- mary pest in Quebec apple orchards, can be naturally parasitized. Knowing that habitats around crop’s peripheries are reservoirs for natural enemies of pests, the objective of the present investigation was to assess parasitism and parasitoid guild composition associated with the OBLR. The two-year study includ- ed orchards under integrated pest management, their edges, and adjacent woodlands. Parasitism was assessed using sentinel OBLR larvae and considered spring, early summer and late summer. Parasitism rates between regions with different vegetation composition were not significantly different. The first year, late summer larvae showed higher parasitism in orchards (27%), compared to edges (7%) and woodlands (11%). The following year, larvae exposed in early summer had higher parasitism rate in edges (28%) compared to orchards and woodlands (17% in both zones). Nineteen parasitoid species parasitized sentinel larvae. The tachinid Actia interrupta (Curran), the most abundant species, represented 28 and 62% of species the first and the second year respectively. Our research demonstrates that natural biological regulation of the OBLR is the result of a highly diversified parasitoid guild and this should be taken into account in any Integrated Pest Management program. Keywords: parasitism, parasitoid diversity, Actia interrupta, larval parasitoid, parasitoid assemblage, species richness, IPM.

[Guilde de parasitoïdes et taux de parasitisme de la tordeuse à bandes obliques dans les vergers de pommiers sous lutte intégrée et dans des boisés adjacents] Choristoneura rosaceana (Harris) [Lepidoptera : Tortricidae] (TBO), ravageur primaire des vergers de pommiers au Québec, peut être naturellement parasitée. Étant donné que les habitats près des péri- phéries des cultures sont des réservoirs pour les ennemis naturels des ravageurs, l’objectif de cette recherche était d’évaluer le parasitisme et la diversité des parasitoïdes de la TBO. L’étude sur deux ans porte sur les vergers sous régie intégrée, leurs lisières et boisés adjacents. Le parasitisme fut évalué avec des larves sentinelles de TBO, placées à différentes périodes (printemps, début, fin d’été). L’année 1, seules les larves de fin d’été ont présenté des différences significatives entre les zones : parasitisme supérieur en verger (27 %), comparativement à la lisière (7 %) et aux boisés (11 %). L’année suivante, les larves exposées en début d’été présentaient un parasitisme supérieur en lisière (28 %), par rapport aux larves en verger et dans les boisés (17 %). Dix-neuf espèces de parasitoïdes ont attaqué les larves sentinelles de TBO. Le tachinaire Actia interrupta (Curran) était le plus abondant (28 % année 1 et 62 % année 2). Nos résultats démontrent que la régulation naturelle de la TBO est le résultat de l’action d’une guilde très diversifiée de parasitoïdes, qui doit être prise en compte dans tout programme de lutte. Mots clés : parasitisme, diversité de parasitoïdes, Actia interrupta, parasitoïdes des larves, assemblage des parasitoïdes, richesse d’espèces, lutte intégrée.

1. Carrefour industriel et expérimental de Lanaudière. 801, route 344, C.P. 3158. L’Assomption, Quebec. Canada. * j.tremblay@ ciel-cvp.ca 2. Laboratoire de lutte biologique. Département de sciences biologiques. Université du Québec à Montréal. 141 Avenue du Président- Kennedy, Montréal, Québec. Canada. * [email protected] 3. Institut de recherche et de développement en agroenvironnement. 335, rang des Vingt-Cinq Est. Saint-Bruno de Montarville, Quebec. Canada * [email protected] 4. Institut de recherche en biologie végétale. Université de Montréal. 4101 rue Sherbrooke Est Montréal, Quebec. Canada * jacques. [email protected] 5. Laboratoire de lutte biologique. Département de sciences biologiques. Université du Québec à Montréal. 141 Avenue du Président- Kennedy, Montréal, Quebec. Canada. * [email protected] 36 PHYTOPROTECTION 98 : 36-45 aim ofthepresentstudy was toassessparasitism Since most orchards in Quebec are under IMP, the organisms areusedinorganic orchards. used duringsummer. Treatments ofkaolinandmicro- are notrelatedtoscouting andpyrethroidsmaybe insecticides. Inconventional orchards,applications two applicationsoforganophosphatesorreducedrisk tion ofanorganophosphate(petalfall),andoneor application ofapyrethroid(duringpink),oneapplica- when neededaccordingtoscouting.Thesecanbeone Management (IPM)considerinsecticidetreatments In Quebec,orchardsunderIntegratedPest parasitoid populations. habitats surroundingorchardsinorder to promote mation isessentialtooptimizeCBC,bymanaging species involved, has never been assessed. This infor associated withorchards,alongtheparasitoid of early-andlate-summerOBLRlarvaeinwoodlands apple fruits(Morinetal.2017).Yet, rates ofparasitism early summer, whichcausessignificantdamageto mid-June. AsecondgenerationofOBLRfollowsin larvae becomeactiveinmid-Mayandremainsountil (Van der Geest and Evenhuis 1991). Overwintering in the 5 the qualityoffruitatharvest,whichattained91% by severalfoldsandresultedinanimprovementof pests inQuebec,increasedparasitoidpopulations planted toattractpredatorsandparasitoidsofapple For example,astudyshowedthatfloweringplants, 1999; Pfannenstielet al. 2010,2012;Unruhet2012). al. 2016; Lavandero et al. 2006; Letourneau and Altieri nutrition sources,andalternativehosts(Gillespieet parasitoid conservation,sincetheyproviderefuges, Wratten enemies (Gillespieetal.2016;Jonsson2008; crop’s peripheryarekeyreservoirsforpest’s natural ber ofstudieshavedemonstratedthathabitatsalong different habitatscontributetoimproveCBC.Anum- understanding ofnaturallyoccurringpestenemiesin et al. 2001).Therefore, an assessment and a better through management of their environment (Eilenberg control (CBC)aimstoenhancenaturalenemyefficacy al. 2012; Unruh nificantly lowerpestpopulations(Pfannenstielet mies ofleafrollers,particularlyparasitoids,cansig- approaches isbiologicalcontrol,sincenaturalene- (Carriére phate andpyrethroidinsecticidesinmanylocations the OBLRhasdevelopedresistancetoorganophos- Quebec appleorchards(Morinetal.2017).However, to NorthAmerica(Beers1993),isaprimarypestin rosaceana (Harris)(Lepidoptera:Tortricidae), endemic The obliquebandedleafroller(OBLR),Choristoneura Introduction and Mcneil2000)itoverwintersas3 The OBLRisbivoltineinsoutheasternCanada(Hunter as parasitoids,whichmayalsoattackapplepests. to woodlandsthatmightharbornaturalenemiessuch 2009). Quebecappleorchardsarefrequentlyadjacent be enhancedbywoodland(BoccaccioandPetacchi et al.2013)andthepersistenceofparasitoidscan tats, atalocalandlandscapelevel(Maalouly on orchardmanagementandtheiradjacenthabi- 2010). Parasitismandparasitoiddiversitydepends th et al. 1998). Such habitats are important for year of this investigation (Bostanian et al.1996).Analternativetochemical et al. 2012). Conservation biological rd instarlarvae et al. - 37 er inwoodlandsthanorchards. Likewise, weexpectedparasitoiddiversitytobehigh- absence ofchemicalinterventionsinthesehabitats. IPM, duetoconditionsfavoringparasitoidsandthe is higherinwoodlandsthanappleorchardsunder hypothesised thatparasitismof sentinel OBLRlarvae cent woodlands,byusingsentinelOBLRlarvae.We parasitoid guildintheseorchardsandtheiradja- of OBLRlarvaeandtocharacterizetheassociated least 1 Missisquoi). Oneexperimentalunit,consistingofat sites inMontérégie-EastandfiveBrome- Missisquoi) and10sitesweresampledin2006(five sites in Montérégie-East and three sites in Brome- Sampling wasconductedat6sitesin2005(three Sampling MATERIALS ANDMETHOS were kepton 1-L watercontainersat1.5 m abovethe apple shoots (10 individuals per apple shoot). These Sentinel larvae were transferred to one-year old Aliniazee 1985). before thecriticluminosity threshold (Gangavalliand the caseoflarvaethathaven’t undergonediapause is present in the naturally occurring population, in vae wereexposedlateinthesummer, as thisinstar parasitoids attackingolderinstars.Fourthinstarlar molt tothirdinstarandbecameacceptablehostsfor exposition period of time (one week) they could instar larvae wereused in spring,since during the smaller andolder/largerhoststoparasitoids.Second as sentinelindividualsinordertoprovideyounger/ instars, aswellfourthinstarlarvae,wereused based onLimabeans(ShoreyandHale1965).Second 5 mL Solo® plastic cups and fed with an artificial diet hatch, first-instarlarvae were individuallyplaced in 5°C untilused(withinthefollowingsevendays).After orchards in2005.Eggmasses≤72holdwereheldat mented withnewoverwinteringlarvaefromthesame and 73°20’36’’O), Quebec.Thisrearingwassupple- mental orchard at Mont-Saint-Bruno (45°32’33’’N (45°31’58.4’’N and73°9’35.91’’E) andinanexperi- in anorganicappleorchardatMontSaint-Hilaire overwintering larvaecollectedduringthe2004spring, ment (IRDA),St-Bruno-de-Montarville, initiated from recherche etdedéveloppementenagroenvironne- ism. TheseoriginatedfromarearingatInstitutde Sentinel OBLRlarvaewereusedtoassessparasit- Sentinel larvae land). and zone(threezones:orchard,theiredge,wood- of OBLRlarvalactivityintheorchard(threeperiods), were thegeographicalregion(tworegions),periods and parasitoiddiversity. Theparametersconsidered Sentinel OBLR larvae were used to assess parasitism dwarf appletreesandpreviousOBLRinfestations. preferred hostplantsbyOBLR,standardandsemi- presence of Cortland and Lobo apple cultivars, known site. Siteswereselectedconsideringthefollowing: land, andtheedgebetweenboth,wasdefinedateach ha orchard under IPM, 1 ha of adjacent wood- - tremblay et al. : parasitoid and parasitism of oblr in ipm in quebec

ground. The basal portion of shoots was in contact from the perimeter. OBLR larvae collected in the with water and their stems and leaves containing orchards were brought to the laboratory and reared sentinel larvae were exposed, providing easy access under the same conditions as sentinel larvae, i.e., for parasitoids to reach sentinel larvae. Each of these until adulthood, emergence of an adult parasitoid or apple shoots on water containers was called a “station”. death.

Region Parasitoid identification Plant composition in woodlands adjacent to orchards All parasitoids emerging from sentinel and indigen- in each region, was characterized visually using a ran- ous OBLRs were preserved in alcohol and iden- dom systematic design (Barbour et al. 1999). Starting tified afterwards using identification keys (Burks from two random points located on the edge between 2003; Goulet and Huber 1993; Grissell and Schauff orchards and woodlands, transects perpendicular to 1990; O’Hara 2005). Identifications were validated this zone were drawn towards the woodlands. On by experts from the Canadian National Collection each transect, two 100 m2 (10 m x 10 m) quadrats of Insects, Arachnids and Nematodes and from the were established at 20–30 m and 50–60 m from the Natural History Museum of Los Angeles County. edge zone. Species belonging to the Rosaceae family, as well as maple sugar, Acer saccharum (Marsh), Calculations and statistical analyses were considered OBLR hosts (Chapman and Lienk 1971; Prentice 1965) and the number of their stems Shannon diversity index (H) (Shannon 1948) for was recorded (as the number of stems available for vegetation, the ratio between deciduous trees and OBLR). The number of conifers and the number of conifers (based on basal area), and the proportion herbaceous plants species in the edge zone were also OBLR host species (based on the number of available noted. stems in the case of trees and based on total surface covered in the case of herbaceous plants) were cal- Periods of OBLR larval activity culated for both, woodlands and edges in each of the two regions, Montérégie-East and Brome-Missisquoi. Assessment of parasitism and parasitoid diversity Student’s t-tests were used to compare these vari- was conducted during three periods of OBLR larval ables between both regions. activity in the orchard in order to represent parasitoid species occurring in each of these periods. The proportion of parasitized OBLR larvae was obtained by dividing the number of total parasitized a) Spring = mid-May to mid-June, at the pheno- larvae by the total of larvae recovered from the sta- logical stages of full pink to post-bloom for tions and suitable for analyses. Several individuals apple trees. were unsuitable for analyses as a result of mortality b) Early summer = early to late July due to causes other than parasitism, which reflect natural mortality excluding parasitism. However, since c) Late summer = early August to early September. the number of larvae suitable for analyses was not the OBLR larvae active in this period enter diapause same in all sites and stations, the improved angular and overwinter as immature larvae. transformation of Johnson and Kotz (1969) was performed in order to adjust parasitism levels (Sokal and Zone Rohlf 1995). The formula for this adjustment is: Three zones or habitats were considered: the orchard, their edge and the adjacent woodland. In 2005, a transect comprising six stations was set up in each of the = arcsin six sites. One station was placed between the orchard and the woodland, in the edge zone. Two stations were placed in the woodland at 20 m and 40 m distance from the edge, and three stations were placed Where y = number of parasitized OBLR larvae in the orchard at 20 m, 40 m and 60 m distance from n = number of recovered OBLR larvae the edge. In 2006 this sampling design was modified suitable for analyses for two transects of three stations: one station in the orchard at 40 m, one station in the edge, and one Total parasitism rates were calculated for each region station in the woodland at 40 m. Ten of each, second- and for each period of OBLR larval activity. Student’s and fourth-instar OBRL larvae, were placed and left t-tests and the Kruskall-Wallis non-parametric test on each of these stations for one week. (SAS institute 2016; Sokal and Rohlf 1995) were used to compare these rates between the regions Assessment of parasitism Montérégie-East and Brome-Missisquoi for each period of OBLR larval activity. After being exposed to parasitism, sentinel larvae were individually transferred to 5 mL Solo® cups and Total parasitism rates in orchards, in edges and in fed ad libitum with a Lima bean artificial diet (Shorey woodlands were calculated for each site and for each and Hale 1965) at 20°C, 16L: 8O, and 60% RH until period of larval activity. Location relative to the edge adulthood, emergence of an adult parasitoid or death. zone (distance from the edge), was not considered a variable affecting parasitism or parasitoid diversity In addition to sentinel larvae, 54 naturally occurring in statistical analyses due to the low number of data indigenous overwintering OBLR larvae were collected found in each location point. on May 16th and 17th 2006 in the 11 orchards from the canopy of apple trees located along the perimeter of Parasitism rates between years were compared by orchards and also from apple trees located at 15 m means of a Chi2 test (α = 0.05) and pairwise com-

38 PHYTOPROTECTION 98 : 36-45 Asterisk indicatestatisticalsignificance(* quoi. Table 1.Vegetation characteristics inwoodlandsandedgesadjacenttoappleorchardsMontérégie-EastBrome-Missis- (A. saccharum). Otherdominantspecieswereblack deciduous treesanddominatedbysugarmaple in Montérégie-Eastwereentirelycomposedof to orchardsineachregionwasdifferent.Woodlands Composition ofthevegetationinwoodlandsadjacent Vegetation ineachregion RESULTS Table exposedtoparasitismintheexperimental sitesinyears2005–2006andparasitismrates.Chi 2.Sentinellarvae software v.13.1 (SASInstitute,Cary, NC). statistical analyseswerecarriedoutusingtheJMP® sitism levels between orchards and woodlands. All performed to examinethe relationship between para- OBLR larvae.However, correlationanalyseswere distribution amongsitesorperiodsofactivity ple sizesdidnotallowstatisticaltestingtocompare roni corrected Chi the threehabitatsforeachgenerationoflarvaeusing Additionally, parasitismrateswerecomparedamong erations ofOBLRlarvae(KleinbaumandKlein2012). performed inordertodetectdifferencesamonggen- parisons, withBonferronicorrectionsofthepvalue Proportion OBLRhostspecies(basedontotalsurface) Shannon diversityindex EDGES Proportion OBLRhostspecies(basedontotalsurface) Shannon diversityindex WOODLANS: herbaceousvegetation Proportion ofOBLRhostspecies(basedonavailablestems) Ratio deciduous/conifers(basedonbasalarea) Shannon diversityindex WOODLANS: trees Parasitized Recovered sentinellarvae Sentinel larvaenotfound Total sentinellarvae 2 Parasitism rate Analyzed larvae Excluded fromanalyses tests.Concerningparasitoidspecies,smallsam- α =0.008). α =0.05) Early summer 13.4% a 149 191 409 600 20 42 39 Montérégie-East (mean ±SE) 2005 0.68 ±0.05 1.50 ±0.29 0.23 ±0.14 1.81 ±0.18 0.78 ±0.06 1.11 ±0.19 0.8629). In2006,springlarvaeshowed8and1.5% in Montérégie-East than in Brome-Missisquoi (t There weresignificantlymorehosttreesforOBLR and northernwhitecedar(ThujaoccidentalisL.). canadensis L.),whitespruce(PiceaglaucaMoench), red pine(PinusresinosaAit.),easternhemlockTsuga species, suchasJackpine(PinusbanksianaLamb.), in Brome-Missisquoiweredominatedbyconiferous poplar (PopulusgrandidentataMichx.).Woodlands raspberry (RubusoccidentalisL.) and thebig-toothed 2.448, Missisquoi, respectively(t were 10.4 and 15.8% in Montérégie-East and Brome- average parasitismratesfor early summerlarvae significant differencesbetweenregions.In2005, (Table 2).Parasitismratesdidnotshowstatistically were parasitizedinyears2005and2006respectively Globally, 15.8and14%ofOBLRlarvaeunderanalyses activity perregion Parasitism associatedtoperiodsofOBLRlarval Missisquoi forlatesummerlarvae(t and 19.7%inMontérégie-East14.9%Brome- 0 Late summer 16.9% a p =0.0419)(Table 1). 1024 1440 307 109 416 52 Brome-Missisquoi (mean ±SE) 0.41 ±0.10 1.38 ±0.26 0.18 ±0.12 1.53 ±0.14 0.56 ±0.07 2.41 ±1.22 1.52 ±0.13 2.5% b Spring 1465 3335 4800 (1.25) 950 515 24 =0.926,p0.499), 2006 (Student’s t-test) (8.46) Early summer =-0.178,p 0.0419* 0.0511 0.7705 0.8125 0.2395 0.1185 21.4% a 2 test(Bonfer 1460 2217 2583 4800 -- p 313 757 (7.53) = - tremblay et al. : parasitoid and parasitism of oblr in ipm in quebec

parasitism in Montérégie-East and Brome-Missisquoi In 2006, parasitism rates of sentinel larvae exposed respectively (H(1) = 0.383, p = 0.536) and there was from mid-May to mid-June (spring), varied from 0 to 20.7% parasitism in Montérégie-East and 23% in 13% among sites and there was no significant differ- Brome-Missisquoi for early summer larvae (t(36.09) = ence among orchards (0.7%), edges (3.4%) and wood- 2 -0.178, p = 0.597). lands (3%) (X (2) = 3.36, p = 0.1862). However, sentinel larvae from early summer showed higher parasitism Parasitism associated to periods of OBLR larval in edges (28%) than in orchards or in woodlands (17% 2 activity per zone in both habitats) (X (2) = 24.29, p < 0.001). In this case, parasitism rates varied from 0 to 50%. Comparisons of parasitism per larval activity period, regardless of zones, indicate that in 2006 spring lar- No significant correlations were found between para- vae had the lowest OBLR parasitism rate, compared sitism in orchards and in woodlands in any of the two to early and late summer larvae in 2005 and to early years. Early summer larvae in 2005: r = -0.027, n = 5, 2 summer larvae in 2006 (X (3) = 108.006, p < 0.0001; p = 0.966; late summer larvae in 2005: r = -0.282, n = Bonferroni corrected α = 0.008) (Table 2). Parasitism 12, p = 0.3742; spring larvae in 2006: r = -0.185, n = 39, levels varied depending on the period of larval activ- p = 0.259; early summer larvae in 2006: r = 0.174, n = ity and the habitat of exposure (Fig. 1). In 2005, para- 39, p = 0.29. sitism rates of 0 to 20% were found in different sites and no significant differences were detected among Parasitism of indigenous OBLR larvae orchards (12%), edges (14%) and woodlands (14.5%) 2 In 2006, 54 naturally occurring overwintering OBLR in early summer larvae (X (2) = 0.1749, p = 0.9168). individuals were found on canopy trees in the 10 However, late summer larvae showed significantly apple orchards considered in this study. Parasitism higher parasitism (27%) in orchards than in wood- 2 rate was 16.7%. lands (11%) or in edges (7%) (X (2) = 16.53, p < 0.001) and it varied from 0 to 54% among sites.

Figure 1. Percentage of parasitized sentinel OBLR larvae in 2005 and in 2006, according to period of OBLR larval activity and zone of exposition (Chi2, p < 0.001).

Parasitoid diversity Regarding diversity of parasitoids, 19 species belong- americanus (Weed) [Hymenoptera: Braconidae], ing to 5 families were recovered from sentinel larvae Colpoclypeus florus (Walker) and Sympiesis sp. during the two-year study (Table 3). The larval para- [Hymenoptera: Eulophidae]. Other species were sitoid, Actia interrupta (Curran) [Diptera: Tachinidae] found occasionally (Fig. 2). Among these, two species was the most abundant species both years. This spe- were found parasitizing the OBLR for the first time in cies was responsible for 4.4% of parasitism in 2005 Quebec, Megaselia longipennis (Malloch) [Diptera: and 8.6% parasitism in 2006. Moreover, A. interrupta Phoridae] and Tranosemella sp. [Hymenoptera: represented 28 and 62% of the parasitoid richness Ichneumonidae]. found in 2005 and in 2006, respectively. Meteorus Concerning indigenous OBLR larvae, they were para- trachynotus (Viereck) [Hymenoptera: Braconidae] (4% sitized by two braconids, Macrocentrus linearis (Nees) in 2005 and 20% in 2006) and Hercus fontinalis and Apanteles sp., causing 13 and 3.7% parasitism (Holmgren) (16% in 2005 and 7% in 2006) were respectively (Table 3). moderately present and followed by Oncophanes

40 PHYTOPROTECTION 98 : 36-45 zone of exposition in 2005 and 2006, and abundance of parasitoid species found in overwintering indigenous OBLR larvae in2005. indigenousOBLRlarvae zone ofexpositionin2005and2006,abundanceparasitoidspeciesfoundoverwintering Table activityineach perperiodoflarval 3.Relativeabundanceofparasitoidspecies(%)foundparasitizingsentinelOBLRlarvae, Macrocentrus linnearis(Nees) Apanteles sp. Braconidae HYMENOPTERA Megaselia longipennis(Malloch) Phoridae Nilea erecta(Coquillet) Hemisturmia parva(Bigot) Compsilura concinnata(Meigen) Actia interruptaCurran Tachinidae DIPTERA Sympiensis sp. Elachertus argissa(Walker) Colpoclypeus florusWalker Eulophidae Oncophanes americanus(Weed) Meteorus trachynotusViereck Bracon politiventris(Cushman) Apanteles sp. Braconidae Tranosemella praerogator(Linnaeus) Itoplectis conquisitor(Say) Hercus fontinalis(Holmgren) Exochus nigripalpisCresson Exochus albifronsCresson Apophua simplicipes(Cresson) Acropimpla alboricta(Cresson) Ichneumonidae HYMENOPTERA Species 10.5 15.8 5.3 5.3 Early summer

Indigenous overwintering OBLRlarvae Indigenous overwintering Orchard 10.5 5.3 5.3 Edge 21.1 10.5 10.5 Woodland 2005 41 7.41 11.1 31.5 1.9 9.3 3.7 1.9

Orchard Late summer 1.9 1.9 1.9 1.9 Edge 1.9 1.9 9.3 13 Woodland 3.7 8.7 13 Orchard Spring 17.4 21.7 4.35 Edge 39.1 4.35 4.35 Woodland 2006 0.64 15.6 1.91 0.64 0.64 0.32 0.32 0.64 1.3 1.3

Orchard Early summer 0.64 33.1 0.64 0.64 5.41 0.32 0.64 1.3 2.9 Edge 1.91 0.32 13.4 0.32 0.64 0.32 0.32 14 Woodland tremblay et al. : parasitoid and parasitism of oblr in ipm in quebec

a) Year 2005

b) Year 2006

Figure 2. Relative abundance of parasitoid species found in parasitized sentinel OBLR larvae in 2005 (a) and 2006 (b) regardless of OBLR generation and zone of exposition.

DISCUSSION

Parasitism Unlike as expected, parasitism rates between Other factors that were not examined in the present regions were not different during the two-year study, study might have affected parasitism rates in wood- even though there were more OBLR tree hosts in lands. These could be landscape fragmentation Montérégie-East than in Brome-Missisquoi. This can- (Elzinga et al. 2007; Kruess and Tscharntke 2000) or not be explained by temperature differences between lack of floral resources for parasitoids in these habi- regions. Brome-Missisquoi was slightly colder than tats (Lavandero et al. 2006; Unruh et al. 2012). Montérégie-East in 2005 and 2006 (Tremblay 2008).

42 PHYTOPROTECTION 98 : 36-45 orchards. Likewise,ourstudy showsawidevariability temperature regimes,andinsecticide managementin ces, suchasalternativeparasitoid hostavailability, ies mightberepresentingdifferences inlocalinfluen- 2004). Suchvariabilityinparasitism ratesacrossstud- our investigation(Brunner 1996; MahrandWhitaker shown higherparasitismrates thanratesfoundin Sackett North America (Li er thanparasitismfoundinsomepreviousstudies Maximum parasitism rate found in this study is high- less ofthezoneandperiodsOBLRlarvalactivity. in 2005and14%totalparasitism2006,regard- exposure. Besides,therewas15.8%totalparasitism 0 and54%,dependingonthesiteperiodof Our studyshowsparasitism rates varyingbetween 26.7°C inJuly2006(Tremblay 2008). with 21.4°C in July and 26.7°C in August 2005, and respectively insamplingsites 2006, contrasting temperature duringMayandJunewere1418.3°C also explaindifferencesinparasitoidactivity. Mean temperatures occurring later in the season, which can occurring duringmid-Maytomid-Junearelowerthan (Pfannenstiel a higheravailabilityofalternativehostsinthisperiod Unruh compared tospring(Cossentineetal.2004,2007; of parasitoidstendstobehigherinlatesummer as 2006. Asotherstudieshavepointedout,abundance mer larvaein2005andearlysummer compared toparasitismfoundinearlyandlatesum- lower parasitismratefoundinspringlarvae2006, summer. Moreover, thisagreeswiththesignificantly parasitoids laterintheseason,comparedtoearly lands toorchardslinkedahigherabundanceof could beduetomobilityofparasitoidsfromwood- summer larvaeofOBLRin2005.Thesedifferences in orchardsthanedgesandwoodlandsforlate early summerlarvaein2006andhigherparasitism edges ascomparedtoorchardsandwoodlandsfor among habitatswerethehigherrateofparasitismin Two exceptionstosimilarratesofparasitismfound tat toanother. in bothhabitatsandmobilityofthesefromonehabi- effect ofanalogoussuitableresourcesforparasitoids in thepresentstudycouldbeattributedtoacombined rates inIPMorchardsandadjacentwoodlandsfound ment-specific differences.Likewise,similarparasitism treated withtoxicinsecticidesmayhavemaskedtreat- combination ofmobilenaturalenemiesandhabitats and reduced-riskinsecticideregimes,statedthatthe leafroller parasitisminorchardsunderconventional Sarvary ural enemieswerenotdifferentinthetwohabitats. authors concludedthat resources requiredby nat- attract alternativehostsforOBLRparasitoids.The such aswildappleandrose(Rosaspp.L.),which harbored a higher abundance of leafroller host plants, habitats weresimilar, evenconsideringthatthelatter sitism rates of OBLR in orchards and in adjacent wild lands. Likewise,Sarvaryetal.(2010)foundthatpara- was foundbetweenparasitisminorchardsandwood- orchards andwoodlands.Moreover, nocorrelation rates andparasitoiddiversitywerefoundbetween since ingeneralnodifferencesregardingparasitism Our resultsdonotconfirmouroriginalhypothesis, et al.2012;Wilkinson2004),mainlydueto et al.2007).Conversely, otherstudieshave et al.(2007b),whoobtainedsimilarresultsof et al.2012).Inaddition,temperatures et al. 1999; Pfannenstiel et al. 2012; 43 Unruh al. 2004;Pfannenstielet2012;Sarvary2010; sitoids ofleafrollersinseveralstudies(Cossentine have previouslybeenmentionedasimportantpara- ids parasitizingtheOBLR(Westbrook 2003).Tachinids State, where this species represented 94% of tachin- A. interrupta. ThisissimilartoratesfoundinNewYork recorded inourstudy, 228(98%)wereidentifiedas occurring parasitoidsspeciesinQuebec. it providesusefulinformationonactivityofnaturally among parasitismratesfromonesitetoanother. Yet, species. research, suggestsacompetitiveadvantageofthe sitoid reportedinthepresentaswellprevious (Cusson and spruceforestineasternUnitedStatesCanada Tortricidae), one ofthemostdamagingpestsfir Choristoneura fumiferana (Lamberth) (Lepidoptera: also amainendoparasitoidofthesprucebudworm, sitoid species(Wilkinsonetal.2004).Thisis in Michigan,A. interruptarepresented13%ofpara- from sentinel OBLR larvae (Sarvary of the three mostabundant parasitoids recovered same authorsshowedthatA. interruptawasone (Sarvary most abundantspeciesinNewYork Stateorchards species in severalregions. For example, this was the has demonstratedtobeoneofthemoreabundant than also widespreadbutoccurredatalowerfrequency fontinalis, in all sitesand generations of OBLR larvae. Hercus A. interrupta wastheonlyspeciesconsistentlypresent Among parasitoid species found in the present study, Tortricidae) andOBLRlarvae. sentinel the sevenspeciesfoundinWashington Stateon found inNewYork State(Sarvaryetal.2007b)and investigation isslightlyhigherthantheninespecies diversity ofparasitoidspeciesshowedinthepresent in orchards,10woodlandsand11edges.The sitizing sentinellarvae.Twelve ofthesewerefound larvae inorchardsandatotalof19werefoundpara- these, twospecieswereassociatedtoindigenous We recorded21speciesparasitizingtheOBLR.From Parasitoid guild conservation biologicalcontrol perspective. izing theOBLR,anditshould befurtherstudiedina A. as informationprovidedby previouswork,showthat lation bythehost.Inconclusion, ourresults,aswell attack ofT. rostrale, triggeringareductioninencapsu - that thisadvantagecouldbeexplainedbyaprevious sitism onsprucebudworm.Theauthorsconcluded (Brishke) (Hymenoptera:Ichneumonidae)forpara- advantage ofA. interruptaoverTranosemea rostrale parasitoid. Cussonetal.(2002)showedacompetitive ately, havingasizeadvantagecomparedtothefirst the eggstage,maggotcanbeginfeedingimmedi- is alreadyparasitized,andthefirstparasitoidstillin maggots searchforthehost(O’Hara2005).If larviposits firstinstarmaggotsnearahostandthe in thereproductivetractoffemale.Thefemale means fertilized eggs are incubated and hatch with- interrupta is a suitable promising species parasit- A. et al. 2012; Westbrook 2003), and interrupta. From the 232 tachinid individuals et al.2002).Abundanceofthistachinidpara- Pandemis pyrusanaKearfott(Lepidoptera: et al.2007aandb).Inanotherstudy, the Actia interrupta M. trachynotusandO.americanuswere is ovoviviparous, which et al. 2010) and A. interrupta et tremblay et al. : parasitoid and parasitism of oblr in ipm in quebec

The parasitoid guild varies depending on OBLR gener- Bostanian, N.J., H. Goulet, J. O’Hara, L. Masner, and ation. Thus, five parasitoid species were present dur- G. Racette. 2004. Towards insecticide free apple ing mid-May to mid-June, when overwintering OBLR orchards: flowering plants to attract beneficial arthro- larvae resume diapause and develop to last larval pods. Biocontrol Sci. Techn. 14: 25-37. Brunner, J. 1996. instars: H. fontinalis, Apanteles sp., M. trachynotus, Discovery of Colpoclypeus florus (Walker) [Hymenoptera: Eulophidae] in apple orchards of E. argissa et A. interrupta. Identification of indigenous Washington. Pan-Pac. Entomol. 72: 5-12. OBLR larvae have confirmed that Apanteles sp. and Burks, R. 2003. Key to the Nearctic genera of Eulophidae, M. linearis parasitize overwintering larvae. Yet, it was subfamilies Entedoninae, Euderinae, and Eulophinae not possible to detect exact time of parasitism occur- (Hymenoptera: Chalcidoidea). World Wide Web electronic rence. However, since Apanteles sp. and M. linearis publication. [http//cache.ucr.edu/%7Eheraty/Eulophidae/] parasitize young larval instars (Cossentine et al. 2005; Accessed on May 4, 2006. Krugner et al. 2005), it is likely that parasitism had Carriére, Y., J.-P. Deland, and D.A. Roff. 1996. Obliquebanded occurred the previous summer. Leafroller (Lepidoptera: Tortricidae) resistance to insecticides: among-orchard variation and cross-resistance. Concerning limitations of our study, according to J. Econ. Entomol. 89: 577-582. Sarvary et al. (2007a), who used the same methodol- Chapman, P., and S. Lienk. 1971. Tortricid fauna of apple in ogy to expose sentinel larvae to parasitism, the water- New York (Lepidoptera: Tortricidae); including an account pick method underestimates natural parasitism but it of apples’ occurrence in the State, especially as a nat- provides an adequate estimation of parasitoid divers- uralized plant. New York State Agricultural Experiment Station, Geneva. Pages 87-90. ity species and demands less resources than using Cossentine, J., A. Bennett, H. Goulet, and J. O’Hara. 2007. potted apple trees. On the other hand, assessment of Parasitism of the spring leafroller (Lepidoptera: Tortricidae) natural enemies by using sentinel larvae might bias complex in organically managed apple orchards in the the results since prey density is abnormal and sen- north Okanagan valley of British Columbia. Pan-Pac. tinel larvae behaviour can be unusual. Nevertheless, Entomol. 83: 276-284. the present investigation gives valuable information Cossentine, J., E. Deglow, L. Jensen, and H. Goulet. 2005. about local occurrence of parasitism on the OBLR, as Biological assessment of Macrocentrus linearis and well as the parasitoid species involved. Apanteles polychrosidis (Hymenoptera: Braconidae) as parasitoids of the obliquebanded leafroller, Choristoneura Parasitism rates, as well as parasitoid diversity found rosaceana (Lepidoptera: Tortricidae). Biocontrol Sci. in this study are relatively similar between habitats. Technol. 15: 711-720. Considering that orchards are habitats disturbed by Cossentine, J., L. Jensen, E. Deglow, A. Bennett, H. Goulet, insecticide treatments, it is likely that woodlands are J. Huber, and J. O’hara. 2004. The parasitoid complex reservoirs for OBLR parasitoids, which are highly affecting Choristoneura rosaceana and Pandemis limitata in organically managed apple orchards. BioControl 49: mobile and can fly to orchards quickly after an insecti- 359-372. cide treatment. Parasitoid activity should be taken in Cusson, M., M. Laforge, J. Régnière, C. Béliveau, D. Trudel, account to orient insecticide management in orchards J. Thireau, G. Bellemare, N. Keirstead, and D. Stolz. and future research. Studies about the impact of 2002. 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