The composition of the egg-parasitoid guild of the golden egg bug, Phyllomorpha laciniata (Heteroptera: Coreidae), in Spain

2019·0.09 MB·

by  David Carrasco

©EntomologicaFennica.17August2012
The composition of the egg-parasitoid guild of the golden egg
bug, Phyllomorpha laciniata (Heteroptera: Coreidae), in Spain
DavidCarrasco&GergelyVárkonyi*
Carrasco,D.&Várkonyi,G.2012:Thecompositionoftheegg-parasitoidguild
of the golden egg bug, Phyllomorpha laciniata (Heteroptera: Coreidae), in
Spain.—Entomol.Fennica23:95–101.
Thegoldeneggbug(Phyllomorphalaciniata(Villers))isaphytophagousinsect
with an unusual reproductive system. Females use the bodies of conspecifics,
bothmalesandfemales,asovipositionsubstrates.Inaddition,avaryingfraction
oftheeggsislaidonthefoodplant.Eggcarryingonconspecificsincreasesoff-
springsurvival.Predatorsand,especially,hymenopteranparasitoidsarethemain
causeofeggmortality.Sofar,onlythewaspGryonbolivari(Giard)(Hymenop-
tera:Scelionidae)hasbeenreportedasaneggparasitoidofP.laciniatainseveral
Mediterraneanpopulations.Inthisstudy,threenewegg-parasitoidspeciesarere-
cordedfromP.laciniata:theprimary solitary parasitoidsGryonmonspeliense
(Picard) and Telenomus sp. (Hymenoptera: Scelionidae), and the facultative
hyperparasitoid Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrti-
dae).Alloftheseparasitoidshavebeenrearedfromhosteggsbeingcarriedby
conspecific bugs. We discuss the taxonomy and biology of the individual
parasitoidspecies,aswellasecologicalandevolutionaryaspectsoftheinterac-
tionsinthishost-parasitoidsystem.
D. Carrasco, Department of Plant Protection Biology, Division of Chemical
Ecology,SwedishUniversityofAgriculturalSciences,P.O.Box102,SE-23053,
Alnarp,Sweden;E-mail:[email protected]
G. Várkonyi (*corresponding author), Finnish Environment Institute, Natural
EnvironmentCentre,FriendshipParkResearchCentre,Lentiirantie342B,FI-
88900Kuhmo,Finland;E-mail:[email protected]
Received26April2011,accepted12August2011
1.Introduction gentea Lam. (Caryophyllaceae). In the labora-
tory,femalesovipositforovertwomonths,laying
The golden egg bug, Phyllomorpha laciniata clutchesof1–3eggseverysecondday(Kaitala&
(Villers,1789)(Heteroptera:Coreidae)isaphy- Miettinen 1997). Individuals are commonly
tophagousinsectdistributedthroughouttheMed- found carrying eggs of different developmental
iterraneanarea(Moulet1995).InSpanishpopu- stagesinthefield.Eggshellcolourationcovaries
lations, females mainly use their conspecifics, with the stage of larval development. Recently
bothmalesandotherfemales,asovipositionsub- laideggsarewhite,thentheygraduallyturnyel-
strates (Kaitala 1996, Kaitala & Smith 2002, lowandeventuallyshinygolden.Nymphsleave
Reguera&Gomendio2002).Yet,someeggscan the carrier directly after eclosion, whereas egg-
also be found on the food plant Paronychia ar- shellsremainattachedtothebodyofthebug.
96 Carrasco&Várkonyi (cid:127) ENTOMOL.FENNICAVol.23
In the wild, eggs laid on plants suffer from ing 2004–2008, was carefully re-examined by
highermortalitythanthosecarriedonbugsdueto oneofus(GV).
predators and, especially, parasitoid wasps Theidentificationliteratureemployedinthis
(Kaitala1996,Reguera&Gomendio2002,Go- study included (i) original descriptions of indi-
mendioetal.2008).Thusfar,onlythescelionid vidualspecies:Giard(1895)forGryonbolivari,
waspGryonbolivari(Giard,1895)hasbeenre- Picard (1924) for G. monspeliense, Mineo &
portedasaneggparasitoidofthegoldeneggbug Szabó(1978)forG.boselliiandMineo(1979a)
indifferentpopulationsinSpain,FranceandItaly for Gryon laraichii; (ii) keys with detailed de-
(Giard 1895, Mineo 1984, Kaitala 1996, Car- scriptionsofspecies:Mineo(1981)toseparateG.
rascoetal.2007,Gomendioetal.2008). bolivarifromG. bosellii, andMineo(1979a)to
Inthisstudy,wereportonafurtherthreeegg distinguish between G. laraichii and G. mon-
parasitoidspeciesassociatedwiththegoldenegg speliense;(iii)revisionsofPalaearcticspeciesof
bugindifferentSpanishpopulationsofP.lacini- Gryon Haliday (Kononova & Petrov 2002,
ata, and discuss their taxonomy and biology as Kononova&Kozlov2008);(iv)arevisionofthe
wellasecologicalandevolutionaryaspectsofthe telenomine wasps (Hymenoptera: Scelionidae:
interactionsinthishost-parasitoidsystem. Telenominae)oftheUSSR(Kozlov&Kononova
1983);and(v)akeytothePalaearcticspeciesof
OoencyrtusAshmead(Trjapitzin1978).
2.Materialsandmethods Morphological terminology follows Mineo
(1980,1981)andMasner(1980,1983).
Adult P. laciniata individuals were collected
from five locations within Spain during 2004–
2008(Table1).Onesamplingsitewassituatedin 3.Parasitoidspeciespool
the Southwest near the locality of El Puerto de
Santa María (Cádiz). The remaining sites were Insect rearing conducted in 2004–2008 yielded
situated in the Northeast near the localities of altogether four egg parasitoid species of P.
Viladecans (Barcelona), El Prat de Llobregat laciniata.Nextweprovidesamplingdataforeach
(Barcelona), Llançà (Girona) and Portbou speciesanddiscusstheirtaxonomyandbiology.
(Girona).Thesitessharedsimilarhabitatcharac-
teristics.Theywereopenareassurroundedbyei-
ther maquis (shrub land) or beach dune habitat, 3.1.Gryonbolivari(Giard,1895)
withsandygravelground,lowandpatchyvege- (Hymenoptera:Scelionidae:Scelioninae)
tation structure and abundant food plant P.
argentea.Collectiondateswereselectedaccord- Materialexamined:
ing to the reproductive period of bugs in each – 1$ El Puerto 10.V.2005, 2$ Cap de Ras
place. 5.VI.2005(det.G.Mineo)
Allparasitoidspecimenswereobtainedfrom – 10# + 6$ El Puerto 1.–10.V.2004, 17# +
theeggscarriedonP.laciniataindividuals.Para- 11$ El Puerto 2.–15.V.2005, 2# + 4$ El
sitizedeggsareeasilydeterminedbytheirblack Puerto 10.V.2005, 1# Cap de Ras 1.–
colouration. We carefully removed parasitized 5.VI.2005,1#+1$CapdeRas5.VI.2005,
eggsfromthebugsusingasmalllabspoon.Para- 1$ Remolar 23.V.2007, 4# + 3$ Remolar
sitizedeggswerestoredinsidesmallvialsforin- 2008,8#+10$Carrabiners2008(det.GV)
cubation in laboratory conditions (26 ± 2 ºC, – 1#+4$ColldelFrare26.V.2006(det.DC)
L17:D7). After eclosion, parasitoids were pre-
servedin70%alcohol. Wefoundagreatervariationinthisspeciesthan
Abatchofrearedparasitoidsobtainedin2005 reported earlier (cf. Mineo 1981, Kononova &
wassenttoGiovanniMineo(Palermo,Italy)and Kozlov2008),inparticularinthelengthratioof
MarttiKoponen(Mikkeli,Finland)foridentifica- postmarginal(pm)andstigmal(st)veinsaswell
tionofscelionidandencyrtidwasps,respectively. as in the length of the longitudinal striae on
Thismaterial,togetherwiththewaspsreareddur- metasomal tergite 2 (T2). In fact, the range of
ENTOMOL.FENNICAVol.23 (cid:127) Egg-parasitoidsofthegoldeneggbug 97
Table1.Localities,samplingyearsofPhyllomorphalaciniataindividuals,andparasitoidspeciesrearedineach
samplingsite.
Samplingsite Coordinates Locality Years Parasitoidspecies
ElPuerto 36°36’N,6°15’W ElPuertodeSantaMaría 2004,2005 G.bolivari
O.telenomicida
Remolar 41°16’N,2°03’E Viladecans 2007,2008 G.bolivari
G.monspeliense
Carrabiners 41°17’N,2°07’E ElPratdeLlobregat 2007,2008 G.bolivari
G.monspeliense
O.telenomicida
CapdeRas 42°23’N,3°09’E Llançà 2005,2006,2007,2008 G.bolivari
G.monspeliense
O.telenomicida
ColldelFrare 42°25’N,3°09’E Portbou 2006 G.bolivari
Telenomussp.
variation in our material partially overlapped coarselysculptured,andthelongitudinalstriaeon
withthatfoundinG.boselliiMineoandSzabó, T2werelonger,thaninlight-colouredspecimens.
1978 (see Mineo 1981, Kononova & Kozlov Thecolourofthemesosomaandmetasomavar-
2008). However, all our individuals shared the ied from almost uniformly red-brown to fully
characterofpossessingshortrowsofminuteteeth black.Alargeproportionofspecimenshadadark
onthemesoscutumalongthelinesofnotauli(re- mesosomabutthecolourofthemetasomaranged
ferredtoas“abbreviatesulci”inMineo(1981); fromred-browntoblack.Femaleshadonaverage
seehisFig.IIonp.121(ibid.)andFig.4onp.237 aslightlyshorterpmthanst,butinafewspeci-
inMineo(1979b)),whichisauniquecharacterof menspmwasequaltoorevenslightlylongerthan
G.bolivari(Mineo1979b,1981). st. In males, pm was usually somewhat longer
Based on (i) the possession of this unique thanst,butwehavealsoseenasinglespecimen
character;(ii)thefactthatvariabilityintheabove withpm<st.Owingtotheconsiderablevariation
mentionedcharactersoccurredascontinuarather ofthesecharacterstatesfoundinG.bosellii,the
than distinct character states; and (iii) that host mostusefulcharactertoreliablyseparatethisspe-
eggsproducingmorphologicallyvariableG.bo- ciesfromG.bolivariseemstobetheabsenceof
livari individuals were sampled from the same theshortrowsofminuteteethonthemesoscutum
carrierbugspecimensonthesamedays,wecon- alongthelinesofnotauli(seeabove).
cludedthatitisnotjustifiedtodivideourreared The known hosts of G. bolivari include
materialintotwospecies,i.e.G.bolivariandG. Phyllomorphalaciniata(e.g.Giard1895,Mineo
bosellii. 1979b,Mineo1984,Kaitala1996,Carrascoetal.
IntheremarksofadescriptionofG.bosellii, 2007), Coreus marginatus (Linnaeus, 1758)
Mineo (1981, p. 126) provides the following (Heteroptera:Coreidae)andanunidentifiedspe-
character states to separatetheseclosely related ciesofRhopalidae(Heteroptera)(Mineo1979b).
species:“G.boselliiistheonlyspecieswhichhas Moreover,Mineo(1979b)postulatedthat,since
inthefemalethepostmarginalisaslongasstig- G. bolivariisalso distributed in areaswhereits
malis. This character and the coarse striae run- knownhostsfailtooccur,G.bolivariwouldpara-
ningonlyinthemiddleofT2forabout¼ofits sitize other coreid species. Gryon bolivari was
length easily distinguish this species from G. fairly abundant and strongly associated with P.
bolivari.Furtheritappearsratherthanconstantly laciniatainallourstudysites(Table1).However,
blackinthebodycolour.”Wefoundthefollow- being an idiobiont parasitoid of heteropteran
ingpatterninourmaterial:specimenswithdark eggs,G.bolivarimayalsoattackalternativehosts
mesosomaandmetasomawereonaveragemore eveninthepresenceofP.laciniata.
98 Carrasco&Várkonyi (cid:127) ENTOMOL.FENNICAVol.23
3.2.Gryonmonspeliense(Picard,1924) speciesintherevisionused.Hence,forthetime
(Hymenoptera:Scelionidae:Scelioninae) being,werefertoitasanunidentifiedspeciesin
thegenusTelenomus.Inanycase,andinspiteof
Materialexamined: thevaguenessofouridentification,wenotethat
– 1$CapdeRas1.–5.VI.2005(det.G.Mineo thisisthefirstrecordofthissubfamily aspara-
asG.laraichii) sitoidsofP.laciniata.
– 1$ Cap de Ras 11.V.2006, 1$ Remolar
29.V.2007, 1# Carrabiners 26.VI.2008 (det.
GV) 3.4.Ooencyrtustelenomicida(Vassiliev,1904)
(Hymenoptera:Encyrtidae)
GryonlaraichiiMineo,1979wasoriginallyde-
scribed in a key couplet (Mineo 1979a) along Materialexamined:
with G. monspeliense. In the same year, Mineo – 1#+1$withoutlabeldata(det.M.Koponen;
(1979b)gaveadescriptionofthisnewspecies,in theremainingmaterial:det.GV)
whichheaddressestheproblemoffailingtofind – 5#+5$ElPuerto1.–10.V.2004
strong morphological differences to separate G. – 1#+1$ElPuerto20.V.2004
laraichii from G. monspeliense. In their recent – 1#ElPuerto2.–15.V.2005
monograph of Palaearctic Scelionidae, Kono- – 1#+1$hatchedfromasinglehostegg,Cap
novaandKozlov(2008)consideredthenameG. deRas28.V.2005
laraichii Mineo to be a junior synonym of G. – 1#+3$(hatched)+1pharate$insidehost
monspeliense (Picard). Hence, we refer to this egg,CapdeRas11.V.2006
speciesasG.monspeliense. – 7$+1pupaCapdeRas25.V.2007
TheknownhostrangeofG.monspeliensein- – 1#CapdeRas01.VI.2007
cludesAeliarostrataBoheman,1852,A.germari – 1#CapdeRas08.VI.2007
Küster,1852(Pentatomidae),Eurygasterintegri- – 2#+2$CapdeRas15.VI.2008
ceps Puton, 1881 (Scutelleridae), Gonocerus – 1$+2#(hatched)+1#insidehostegg+1
acuteangulatus (Goeze, 1778) (Coreidae) (Mi- pharate adult inside host egg, Carrabiners
neo1979a,b,Kononova&Kozlov2008)andP. 2008
laciniata(Coreidae)(newhostrecordaddedhe- – 4# + 16$, (specimens without label data)
re).Gryonmonspelienseseemstobeafairlyrare 2008
butconstantmemberoftheegg-parasitoidguild
ofP.laciniatainnortheasternSpanishstudysites ThisspecieshasavastdistributionareafromGer-
(Table1).Phyllomorphalaciniataisprobablynot manyinthenorthtoSyriaandIraninthesouth,
themainhostofthisspecies. and from Spain, Portugal and Morocco in the
west to eastern China in the east (Noyes 2001,
Zhangetal.2005).Ooencyrtustelenomicidahas
3.3.Telenomus(Telenomus)sp. averywidehostrangecomposedofmanyspecies
(Hymenoptera:Scelionidae:Telenominae) inmainlyheteropteran(Coreidae:6spp.,Penta-
tomidae:18spp.,Pyrrhocoridae:1sp.,Reduvii-
Materialexamined: dae:1sp.,Scutelleridae:3spp.)andlepidopteran
– 1#+1$ColldelFrare26.V.2006 (1sp.ineach:Lasiocampidae,Lymantriidae,No-
todontidae,PapilionidaeandSphingidae)famili-
We used the revision of the subfamily Teleno- es (Noyes 2010). Phyllomorpha laciniata is a
minaebyKozlovandKononova(1983)inourat- newcoreidhostforthisspecies.Therearealsoa
tempttoidentifythisspecies.Althoughitisevi- fewrecordsofprimaryegg-parasitoidhostsofO.
dentthatitbelongstothespecies-richsubgenus telenomicida in the hymenopteran genera Tris-
Telenomus of the genus Telenomus Haliday, solcusAshmeadandTelenomusHaliday (Sceli-
1833,thisspeciesdidnotfitthedescriptionofany onidae:Telenominae:Telenomini)(Noyes2001).
ENTOMOL.FENNICAVol.23 (cid:127) Egg-parasitoidsofthegoldeneggbug 99
4.Interactionbetweenparasitoids Ooencyrtus venatorius De Santis & Vidal
Sarmiento,1976, O. venatorius was a generally
Accordingtotheliterature(seeNoyes2001and moresuccessfulcompetitorthanT.costalimaiaf-
referencestherein),O.telenomicidaisaprimary ter nearly simultaneous oviposition by the two
eggparasitoidora(facultative)hyperparasitoid. parasitoid species. Another example of a host-
This species was abundant in both the southern multiparasitoidcommunityengagingOoencyrtus
andthenortheasternstudyareasanditfrequently was studied in California (e.g. Amarasekare
coexistedwithG.bolivari(Table1).Aswehave 2003). In that system, Trissolcus murgantiae
nodirectobservationsofparasitismofG.bolivari Ashmead, 1893 and Ooencyrtus johnstonii
byO.telenomicida,thenatureoftheirinteraction (Howard, 1898) both attack the eggs of the
might be competition over eggs of P. laciniata, pentatomidharlequinbugMurgantiahistrionica
hyperparasitism,orboth. (Hahn,1834).Ooencyrtusjohnstoniiisagregari-
UnlikethescelionidparasitoidsofP.laciniata ous and superparasitic species competing with
eggs, which developed as solitary parasitoids, thesolitaryT.murgantiaeforhosteggs,andthe
eggsattackedbyO.telenomicidasometimespro- latter parasitoid is superior in this exploitative
ducedtwoadultparasitoids(seesection3.4.)that competition.Ithasalsobeenshownthatinterac-
were smaller than their solitary conspecifics. tionbetweenthesecoexistingparasitoidspecies
Moreover,allP.laciniataeggshostingO.teleno- dampens host population fluctuations (Amara-
micidacontainednumerousundevelopedeggs.A sekare2003).
potential explanation for this phenomenon is
superparasitismby (differentfemaleindividuals
of) O. telenomicida. An alternative mechanism, 5.InteractionbetweenP.laciniata
i.e.ovipositionofseveraleggsbyasinglefemale anditseggparasitoids
parasitoid,isknownfromseveralkoinobiontlar-
valendoparasitoids (seeGodfray 1994 for are- Itisimportanttounderlinetheevolutionary-eco-
view).Suchbehaviourmightbefavouredbyse- logical significance of our new rearing records
lectionasitmayexhaustthecellularimmunere- from the viewpoints of both the host and the
sponse of the host. However, in idiobiont parasitoid species. Parasitoids act as selective
parasitoidssuchasO.telenomicida,layingsev- pressureontheirhosts.Asaresult,newadapta-
eraleggsinasinglehosteggprobablywouldnot tionsmayariseinthehostspeciesinordertomin-
be similarly beneficial. Nonetheless, at present imizetheriskofparasitism.Ithasbeensuggested
wehavenomeanstovalidateeitherofthetwoal- that oviposition on conspecifics in P. laciniata
ternativehypotheses. mayrepresentastrategytoreducepredationand
Gregariousdevelopmentiswidelyknownto parasitismoftheeggs(Kaitala1996,Reguera&
occur in Ooencyrtus species. For instance, O. Gomendio2002,Carrascoetal.2007,Gomendio
nezaraeIshii,1928hasbeenreportedtoparasit- etal.2008,Carrasco&Kaitala2009,Carrasco&
ize four species of phytophagous bugs in Japan Kaitala 2010). The new parasitoid records re-
andtodevelopasagregariousparasitoidinoneof portedinthisstudyincreasemarkedlythediver-
them (Mizutani et al. 1996). This parasitoid is sity ofparasitoidspeciesfoundtobeassociated
usuallysolitaryinasmallhostbutgregariousina withP.laciniataeggs.Theseresultsgivefurther
large host (Takasu & Hirose 1991), suggesting supporttothehypothesisthateggparasitoidsplay
thatthesizeofprogenydependsonbothhostsize animportantroleintheovipositionstrategyofP.
and the outcome of competition following laciniata females, and may help to explain the
superparasitism. Superparasitism is in fact very evolution of such unusual behaviour. Neverthe-
common in O. nezarae (e.g. Takasu & Hirose less, additional investigations should be con-
1991).Inasimilarhost-parasitoidsystemfound ductedtotestthishypothesis.Forinstance,there
inVenezuela(Conde&Rabinovich1979),con- is a need to assess the incidence of individual
sisting of eggs of the reduviid bug Rhodnius parasitoidspeciesinP.laciniataeggsinvarious
prolixus Stål, 1859 and their parasitoids Tele- populations.Itmaybeinterestingtostudyfurther
nomus costalimai Ortiz & Alvarez, 1959 and (see Gomendio et al. 2008) the relationship be-
100 Carrasco&Várkonyi (cid:127) ENTOMOL.FENNICAVol.23
tween the incidence of egg-parasitism and the Carrasco,D.,Borg,Å.A.&Kaitala,A.2007:Egg-laying
ovipositionstrategyofP.laciniataamongpopu- inrelationtoeggsubstrateinGryonbolivari,anegg
parasitoidofthegoldeneggbug(Phyllomorphalaci-
lations,especiallythoseinwhichfemaleegg-lay-
niata).—JournalofInsectBehavior20:307–313.
ingbehaviourdiffersfromovipositingprimarily
Carrasco,D.&Kaitala,A.2009:Egg-layingtacticinPhyl-
on conspecifics (e.g. Kaitala 1996, Reguera & lomorphalaciniatainthepresenceofparasitoids.—
Gomendio 2002, D. Carrasco, S. Kivelä & A. EntomologiaExperimentalisetApplicata131:300–
Kaitalaunpubl.)byovipositingmostlyonplants 307.
Carrasco,D.&Kaitala,A.2010:Activeprotectionofun-
and other substrates (e.g. Mineo 1984, D.
relatedoffspringagainstparasitoids.Abyproductof
Carrasco,L.Härkönen&A.Kaitalaunpubl.).
self defense? — Behavioral Ecology and Sociobio-
ApreviousstudyshowsthatP.laciniataindi- logy64:1291–1298.
vidualscounteractmostoftheattemptsofG.boli- Conde,J.E.&Rabinovich,J.E.1979:Larvalcompetition
varitoapproachtheeggstheycarry(Carrasco& betweenTelenomuscostalimai(Hymenoptera:Scelio-
nidae)andOoencyrtustrinidadensisvenatorius(Hy-
Kaitala2010).Theauthorssuggestthatthemere
menoptera: Encyrtidae) after simultaneous oviposi-
fact of egg carrying and the behavioural re-
tioninRhodniusprolixuseggs(Hemiptera:Reduvii-
sponses bugs display against parasitoids may dae).—JournalofMedicalEntomology16:428–431.
considerablydecreasetherateofsuccessfulegg Giard,A.1895:Surquelquesespecesnouvellesd’Hymé-
parasitization and increase the length of the noptèresparasites.—BulletindelaSociétéEntomo-
logiquedeFrance(1895):74–78.
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Godfray,H.C.J.1994:Parasitoids.Behavioralandevolu-
timecostinparasitizingtheeggscarriedbybugs
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niataisfavouredbynaturalnotsexualselection.—
(particularlyG.bolivari,G.monspelienseandO.
AnimalBehaviour75:763–770.
telenomicida) that parasitize eggs carried on P.
Kaitala,A.1996:Ovipositiononthebackofconspecifics:
laciniataremainsunclear.Furtherstudiesonthis Anunusualreproductivetacticinacoreidbug.—Oi-
host-multiparasitoid system should investigate: kos77:381–389.
(i)thehostlocationmechanismofeachparasitoid Kaitala,A.&Miettinen,M.1997:Femaleeggdumping
andtheeffectofsexratioonmaleeggcarryinginaco-
species; (ii) the interaction between coexisting
reidbug.—BehavioralEcology8:429–432.
parasitoid species; and (iii) whether these para-
Kaitala, A. & Smith, R. L. 2002: Do golden egg bugs
sitoidsgainsomefitnessbenefit,suchasreduced (Phyllomorphalaciniata:Heteroptera,Coreidae)re-
predation or reduced superparasitism and/or quireconspecificsforoviposition?—JournalofIn-
hyperparasitism, by exploiting the egg-carrying sectBehavior15:171–180.
Kononova,S.V.&Petrov,S.2002:(Reviewofthegenera
anddefensivebehaviourofadultP.laciniata.
GryonandExon(Hymenoptera,Scelionidae)ofthe
Palaearctic.2.AkeyforidentificationofGryonspe-
Acknowledgements. We are grateful to Martti Koponen ciesandareviewofthegenusExon).—Zoologiches-
andGiovanniMineoforidentifyingsomeoftheparasitoid kyZhurnal81:53–59.[InRussian.]
material.WewishtothankGavinBroadandananony- Kononova,S.V.&Kozlov,M.A.2008:(Scelionidsofthe
mousrefereefortheirvaluablecomments.Specialthanks Palearctic (Hymenoptera, Scelionidae). Subfamily
to “Consortium of the Natural Areas of Delta del Scelioninae).—TovarishchestvoNauchnykhIzdanij
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help during field work. Finnish Cultural Foundation, pp.[InRussian.]
Oskar Öflunds Stiftelse, CIMO Fellowships and Alfred Masner,L.1980:KeytothegeneraofScelionidaeofthe
KordelinFoundation(grantstoDC)supportedthisstudy. Holarcticregion,withdescriptionsofnewgeneraand
species(Hymenoptera:Proctotrupoidea).—Memoirs
oftheEntomologicalSocietyofCanadaNo.113:1–
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