Immature stages of Aganaspis pelleranoi (Brèthes) (Hymenoptera: Cynipoidea: Eucoilidae), a parasitoid of Ceratitis capitata (Wied

7 Pages·1994·2.2 MB·English

by  S M Ovruski

HYM. RES.
J.
Vol. 3, 1994, pp. 233-239
Immature Stages ofAganaspis pelleranoi (Brethes)
(Hymenoptera: Cynipoidea: Eucoilidae),
a Parasitoid of Ceratitis capitata (Wied.)
and
Anastrepha Spp. (Diptera: Tephritidae).
Sergio M. Ovruski
CentredeInvestigaciones para la Regulationde PoblacionesdeOrganismosNocivos(CIRPON), Pasa|eCaseros 1050,
C.C.C. 90,S. M. deTucuman (4.000), Argentina.
—
Abstract- Theembryological-larvaldevelopmentofAganaspispelleranoi(Brethes),alarvalparasitoidofCeratitiscapitata
(Wied.)andAnastrephaspp. isdescribedand illustrated. A. pelleranoipossessesastalkedegg,eucoiliform first-and second-
instarlarvae,andhymenoptenformthird-andfourth-instarlarvae,followedbyaprepupaland pupalstage.Thedurationof
eachstageat25-26°Cwasasfollows:egg,3-4days;first-,second-,and third-instarlarvae,2-3dayseach; fourth-instarlarva,
3-4days, prepupa, 1-2days; pupa,9-14days.
Aganaspispelleranoi(Brethes)isaparasitoidof MATERIALS AND METHODS
Ceratitis capitata (Wied.) and several Anastrepha
species (Diptera: Tephritidae) in Argentina (De Aganaspis pelleranoi was reared on last instar
Santis 1965), that attacks the final larval instar of larvaeofC. capitata in the laboratory as described
thesefruitflies(TuricaandMallo1961).Aganaspis byOvruski(inpress).Thehostlarvaewerereared
pelleranoi has also been reported from Lonchaea on carrot/corn meal/yeast medium as described
spp. (Diptera: Lonchaeidae) in Brazil (De Santis by Nasca (1977).
1980). The life cycle and immature stages of A.
From 1941 to 1945, A. pelleranoi was released pelleranoi were studied by exposing 20 to 30 C.
as a control agent of fruit flies in Tucuman prov- capitata larvae to individual parasitoid females.
ince, Argentina (Nasca 1973). In 1942 this species Therearingsandexperimentationwereconducted
wasintroducedand reared in Peru forthecontrol at25-26°C,70-80%RH,and12:12LDphotoperiod.
ofA.fratercuhts (Wied.) (Clausen 1978). Host larvae and host puparia were removed at
Ovruski (inpress)carried outstudies onhost intervals of24 h after parasitism and dissected in
detection behaviour in this fruit fly parasitoid. Insect Ringer's solution ondepression slides. The
Otherwise little is known of the biology of A. parasitoid larvae were removed from each host
pelleranoi,anddescriptionsoftheimmaturestages puparium and preserved in 70% ethanol for later
of this species have not been published. In fact examination by light microscopy. Eight fourth-
verylittleatallispublishedonthedevelopmentof instar larvae were refixed in 4% glutaraldehyde
M
eucoilid parasitoids of fruit flies, except that and0.2 phosphatebuffer,anddehydratedin35-
Clausen et al. (1965) briefly described the imma- 50-70-90-100%ethanol.Thereaftertheywereplaced
ture stages of A. daci (Weld) (=Trybliograplia daci in 100% acetone. These specimens were critical
Weld), a parasitoid of Dacits dorsalis Hendel, the point dried beforeexamination by scanning elec-
oriental fruit fly. tronmicroscopy(SEM). Descriptionsarebasedon
Inthispaper,studiesonthelifecycleandpre- several specimens. Thirty-four eggs in different
imaginal development of A. pelleranoi are pre- stages of development were mounted on slides
sented. and examined by light microscopy. Six first-, five
234 Journalof Hymenoptera Research
second-,andfivethird-instarlarvaeweremounted formed. Thestalkdisappears (Fig. 4 )and thesize
and examined by light microscopy. Eight fourth- oftheeggissimilartothe48holdegg. Eclosionof
instarlarvaewereobserved withSEMand fifteen the first-instar larva occurs after 78-80 h. The
fourth-instar larvae were examined by light mi- chorion isbroken throughanteriorlyby theman-
croscopy. Six females of A. pelleranoi of different dibles and posteriorly by movements of the tail
ages were dissected in Insect Ringer's solution to (Fig. 5 ).
observe the ovarian matureeggs. The terms used
formorphologicalstructurefollowKopelmanand LARVAL DEVELOPMENT
Chabora (1984) and Evans (1987). The drawings
were made with a camera lucida. Data are pre- After hatching, the first-instar larva actively
sentedasrangeand/ormean.Specimens,inetha- feeds on the internal tissues of the host. For this
nol and mounted, are deposited in the Miguel purpose, the mandibles are protruded from the
Lillo Institute Fundation, S. M. de Tucuman Ar- oralcavity, although it was not possible to verify
gentina. theiruseinfeedingby directobservation. During
thisstage,thetailbecomeslessprominentand the
LIFE CYCLE head wider.
Thesecond-instarlarvaappearsonthefifthto
FemalesofA.pelleranoidepositedasingleegg sixth day after oviposition, when the host pu-
in thebodycavity of the host larva and one para- parium is formed. The larva continues to feeds
sitoid adult emerged from each host puparium. inside thehost pupa.
Underlaboratoryconditions, theperiod from The third-instarlarva appears on the eigth to
ovipositioninthehostlarvatotheemergenceofa ninth dayafteroviposition. In thisstage thepara-
parasitoidadultvariedfrom25to27daysinmales sitoid larva partially emerges from the host pupa
and from 26 to 30 days in females. Thus, males near the middle region, and it then feeds exter-
tended toemergesomewhatearlierthan females. nally within the host puparium. The parasitoid
Theeggstageinsidethehostlarvalasted about3- larva occupies both internal and external posi-
4 days. Observations of the postembryological tions in the host pupa and develops two respira-
development showed the presence of four larval tory mechanisms: cuticular respiration through
instars. The first, second, and third instar each submerged posterior parts of the body and tra-
lastedabout2-3daysandthefourthinstar3-4days cheal respiration through prothoracic spiracles.
(9-13days in total). The prepupal stage lasted 1-2 In the fourth-instar larva, which appears on
days, and the pupal stage from 9 to 14 days. approximately the tenth day after oviposition,
feeding continues externally on what remains of
EMBRYOLOGICAL DEVELOPMENT the host pupa. The parasitoid larva is very slug-
gishandoccupies3/4ofthehostpuparium. After
mm
Thenewly laid eggis 0.32mm-0.56 long feedingiscompleted, themeconiumisreleased.It
mm mm mm
and 0.m06m -0.10 wide; thestalkis0.42 appearsasadarkcrustintheposteriorapexofthe
- 0.73 long and the embryo is not yet distin- puparium (Fig. 14 ).
guishable (Fig. 1).
24hafterovipositioninsidethehostlarva,the DESCRIPTIONSOF IMMATURE STAGES
mm
parasitoid egg is0.26mm-0.48 long and 0.08 —
mm mm
-0.15 wide.Thestalkisreducedinlength, Mature ovarian egg. (Fig. 1.) Stalked; total
and the embryo, vitelline membrane and the lengthonaverage0.60mm;stalk1.2Xlongerthan
chorion are well discernible (Fig. 2 ). eggbody,thelatterportion3.5Xlongerthanwide;
By 48 h after oviposition, the egg has length- chorion translucent and smooth.
mm
enedandswelled(0.52mm-0.66 longand0.24 —
mm mm mm
- 0.26 wide), and thestalkhas decreased First-instarlarva. (Fig. 6,7). Length0.93
still more (Fig. 3 ). The embryo shows signs of - 1.39 mm; 2.2 X longer than wide; eucoiliform;
bodysegmentation,acaudalportionand thoracic translucent;subcylindricalinshapewithelongate
appendages. distinct head; mouth surrounded by several oral
After 72 h the parasitoid larva is completely papillae, inside with a pair of unidentate
Volume 3. 1994 235
1
Figs. 1-7.Aganaspispelleranoi.1,ovarianegg.St.,stalk.Scalebar=0,12mm.2,eggat24h.afteroviposition.ch.,choIrion; V.M.,
vitellinemembrane;Em.,embryo.Scalebar=0,12mm.3,eggat48h.afteroviposition.Scalebar=0,12mm.4,eggat72h.after
oviposition.Scalebar=0,12mm.5,eggat80h.afteroviposition.Scalebar=0,12mm.6,first-instarlarva.OP.,oralpapillae;
Th.App.,thoracicappendages;V.P.,ventralprocess;77.,tail;An.,anus.Scalebar=0,12mm.7,mandiblesoffirst-instarlarva.
Scalebar= 0,02 mm.
236 Journalof Hymenoptera Research
n.
Ml.
G. F.
Figs.8-9.Aganaspispelleranoi.8,second-instarlarva.OP.,oralpapillae;77.,tail.Scalebar=0,25mm.9,third-instarlarva.Sp.
spiracle;Mt.,mouth; C.F., globularfat;An.,anus.Scalebar=0,32mm.
237
Figs.10-12.Aganaspispelleranoi.10,fourth-instarlarva.Lat.Sw.,lateralswelling;An.,anus.Scalebar=1,0mm.11,anteriorvmimew
ofhead,fourth-instarlarva.Ant.Or.,antennalorbit;Ma.,mandible;Mi.,maxilla;La.,labium;Lb,labrum.Scalebar=0,10
12, lateralviewofbodysegment6-8, fourth-instarlarva. Sp, spiracle; Lat Sw, lateral swelling. Scalebar = 0,10mm.
subtriangular mandibles (Fig. 7 ); ventral surface ment with very short tail and without ventral
of head with a prominent tubular projection; gut process; anus opening dorsally.
easily discernible; each thoracic segment with a —
mm-
pair of long slender ventral appendages; seven Third-instar larva. Fig. 9. Length 2.78
well-definedabdominalsegments;caudalsegment 3.45 mm; 3 X longer than wide; more typically
with a long tail and short ventral process; tail hymenopteriform; yellowish with several white
bearing several small setae apically; ventral mar- globular fat particles in thorax and abdomen; cy-
gin of 7th abdominal segment and basal end of lindrical in shape with slender posterior portion;
caudalsegmentwithscalelikeornamentation;tail broadhead;smallunidentatemandibles,difficult
6 X longer than ventral process; anus opening todiscern; prothoracicsegment with asinglepair
dorsally. of spiracles; ten distinguishable body segments;
— brain and gut easily discernible; without tail and
mm
Second-instarlari'a. (Fig. 8). Length 1.53 ventral process; anus opening ventrally.
- 2.31 mm; 2 X longer than wide; modified —
eucoiliform; whitish yellow with some white Fourth-instarlarva. Figs.10,11,12,13).Length
globular fat particles; cylindrical in shape with 3.48 mm-4.13 mm; 2 X longer than wide;
short and fleshy head; mouth with external oral hymenopteriform;whitishyellowwithmanysmall
papillae; unidentate mandibles; gut well discern- whiteglobularfatparticlesdispersed throughout
ible; without thoracic appendages; caudal seg- dorsolateral parts of thorax and abdomen; head
23S Journalof Hymenoptera Research
13
Me.
Figs. 13-15. Aganaspis pelleranoi. 13, mandibles of fourth-instar larva. Scale bar = 0,04 mm. 14, prepupa inside the host
pupanum. Ph.,pupanum; Pr., prepupa;Me,meconium.Scalebar = 1,0mm. 15, pupa. Scalebar= 1,6mm.
relativelylarge,subcircularinfrontview,without instar larva; body curved and reduced in size;
setae; antennal orbits large; prominent bidentate occupying 2/3 of the host puparium.
mandibles, 1.2 X broader than long basally, very
mm
darkapically(figs.11and13);labrum3.2Xbroader Pupa.— (Fig. 15). Length 2.68 - 2.99 mm,
thanlong, with rounded lateral sidesand median minimtially wmhimte, laterbecoming dark; antennae 1,7
depression on apical margin; maxillae circular in -2.1 in length,extendingtofirstabdomi-
shape and joined to labium; body very swollen; nal segment.
only eleven body segments discernible; except
prothoracic and terminal abdominal segment, all DISCUSSION
segments with a pair of spiracles; each body seg-
mentprovidedwithlateralvoluminousswellings Aganaspis pelleranoi produces a stalked egg,
behindspiracles(Fig. 12);integumentsmoothand typical of the Eucoilidae. The transition from en-
without setae; anus opening ventrally. doparasitic to ectoparasitic life has also been re-
mm ported forotherspeciesofEucoilidae (Jenni 1951;
Prepupa.— (Fig. 14). Length 2.55 - 2.98 Wishart and Monteith 1954; Sychevskaya 1974;
mm
mm; width 1.18 - 1.56 mm; similar to fourth- KopelmanandChabora 1984).Theembryological
Volume 3, 1994 239
andlarvaldevelopmentissimilartoothereucoilid Book, N°480. 545 pp.
parasitoids:Tn/bliograpliarapae(Westwood)(James Clausen,C.P.,D.W.ClancyandQ.C.Chock.1965.Biological
1928; Wishart and Monteith 1954); Hexacola sp. caonndtrtohleofotthheerofrriueinttaflliefsruiitnfHlyaw{aDiaic.usTedcorhsnailciaslHBeunldleetli)n
(Simmonds 1952); Hexacola sp. near Websteri UnitedStatesDepartmentofAgriculture,N"1322. 102pp.
(Crawford) (Eskafi and Legner 1974); Leptopilina De Santis, L. 1965. Nota sobre un parasito de la mosca
boulardi (Barbotin et al.) (Kopelman and Chabora sudamencana de la fruta (Hymenoptera: Cynipidae).
1984); Eucoila frichopsila (Hartig) (Sychevskaya Rei'istadelaSoaedadEntomologicaArgentina27(1-4):73-
74.
1974) and Kleidotoma japonica Huz. (Huzimatu DeSantis,L. 1980.Catalogodeloshimenopterosbrasilenos
1940). de la Sene Parasitica, incluyendo Bethyloidea.
Clausen et al. (1965) reported three larval in- UniversidadFederaldoParana, Curitiba. 395pp.
ofstnoadur-rs,liaanrnAvd.alfdaoicunirstt.ahTr-hsiinsisntsaAtr.uldpayerlpvlearreoavndoeeiss.ctTrhihebeperdfeirhsseet-rn,ecseaeroce-f EskafisH(,iEtpuaFp.cgeoeMlis.altiaenonsafede:tyEh.eHeyFg.mncLeayentngosnipep(triDe.dirp1at9H)e7er,4ax.:aaDcCelohsallcraorvriaosplppt-.iipodunapnseael)ao.rfpiaTrWmhaeemsbaiCsttateunerraoei-f
similar to the first-, second-, and supposed third- dian Entomologist 106: 1043-1048.
instar larvae of A. daci respectively. The third- Evans, H. E. 1987. Cynipoidea. Cynipids, gall wasp and
itnhsetaerulcaorivlaiefoorfmA.tpyepleleraanndoiitshaethryanmseintoiopntbeertiwfeoernm HuzimoKtaehtneudra,sl,lKp.pH.u1n964t60,5.-D6T6uh.beuInqluiSfetee,hhrIi,sotwFoa.r.Wy.7,o5f4edap.pn.Iemwmatcuyrneipiindsecftlsy.,
type.Thisstageisdistinguishedbyasinglepairof Kleidotomajaponica,n.sp.ScienceReport,TobokuImperial
open spiracles, in the prothoracic segment, as in University,Sendai15:457-480.
the supposed third stage of T. rapae (Wishart and James,H.C.1928.Onthelifehistoriesandeconomicstatusof
Monteith 1954), the supposed fourth stage of £. coefrstaoimnepanreawsitleasrvoafldfioprtmesr.oAunsnlaalrsvaoef,AwpipltiheddeBsicorliopgtyio1n5s:
frichopsila (Sychevskaya 1974) and the supposed 287-316.
fourthstageofL.boulardi(KopelmanandChabora Jenni, W. 1951. Beitrag zur Morphologie und Biologie der
1984).Furthercomparativeworkwouldbeneeded CynipidePseudeucoilaboclieiWeld,eineslarvenparasiten
to confirm these apparent differences between vonDrosophilamelanogasterMeig.ActaZoologica32:177-
254.
species,asintermediateinstarsofapocritanlarvae Kopelman,A.H.andP.C.Chabora.1984.Immaturestagesof
arenotoriously easy to overlook. Leptopilina boulardi (Hymenoptera: Eucoilidae), a
Furthermore Clausen et al. (1965) stated that protelean parasite of Drosophila spp. (Diptera:
the first-instar larva ofA. daci does not possesses Drosophilidae). Annals of the Entomological Society of
discerniblemandibles,butthefirst-instarlarvaeof America77(3):264-269.
A.pelleranoihasapairofwelldevelopedunidentate Nascae,stJa.blAe.cid1o9s73.enPaarl^gsuintaoss zdoena"smodsecaTsucduem^lnos. fRreuvtiosst"a
mandibleswiththeirendsprojectingfromtheoral AgricoladelNoroeste Argentino 10(1-2):31-43.
cavity, similar to the first-instar larvae of £. Nasca,J.A.1977.Estudiosrelacionadosconlasposibilidades
del Control Integrado de las moscas de las frutas.
trichPoprsoimlain(eSnytchbeivdseknatyatae1m97a4n)d.ibles in last instar 5U2n9i.ve6r1sipdpa.d Nacwnal de Tucumdn, Informe CAFPTA, N"
larvaehavealsobeenreportedforA.daci(Clausen Ovruski,S.M.Inpress.Comportamientoenladetecciondel
et al. 1965), Trybliograplia Forster and Hexacola huespedenAganaspispelleranoi(Brethes)(Hymenoptera:
Fbrster (Evans 1987). Cynipoidea,Eucoilidae)parasitoidedelarvasdeCerafitis
capitata (Wied) (Diptera: Tephritidae). Revista de la
ACKNOWLEDGMENTS SociedadEntomologicaArgentina53.
Simmonds,F.J.1952.Parasitesofthefrit-fly,Oscinellafrit(L.),
in eastern North America. Bulletin Entomological Re-
IamespeciallygratefultoDr.PatricioFidalgo(CIRPON, search43: 503-542.
Argentina), Dr. Abraham Willink (CONICET-UNT, Argen- Sychevskaya, V. L. 1974. The biology of Eucoila trichopsila
tina), and Dr. Goran Nordlander (Swedish University of Hartig (Hymenoptera, Cynipoidea), a parasite of the
AgriculturalSciences,Uppsala,Sweden)forsuggestionsand larvaeofsynanthropicfliesofthefamilySarcophagidae
critical reviewsofthemanuscript Turica(,DipAt.eraan).dERn.toGm.olMogailclaol.R1e9v6i1e.wO5b3s:e3r6v-a44c.iones sobre la
poblaciondelas "Tephritidae" ysusendoparasitoides
LITERATURE CITED en algunas regiones citricolas argentinas. IDIA 6: 145-
161.
Clausen,C. P. 1978.Tephritidae,pp.320-334.In Clausen,C. Wishart,G.andE.Monteih.1954.Trybliograpliarapae(Westw.)
P., ed.IntroducedParasitesandPredatorsofarthropod (Hymenoptera: Cynipidae), a parasiteofHylemya spp.
pestsandweeds:aWorldReview.U.S.AgricultureHand (Diptera: Anthomiidae). The Canadian Entomologist 86:
145-154.