TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan eetua Lqpidopte]uScienc'6e2(4)1:51-155,December 2011 A record of a koinobiont endoparasitoid wasp, Melatophacharops everese (Hymenopte Ircah,neumonidae), lycaenidbutterflAyq,ytolepis attacking eggs of a puspa Masnmi SHIMAzAKIi )K"y,ohei WAmNABE2) and Ybshiko SHIMAzAKIi) i)440-114Matsunanii-choT,akasago-cho,TakasagoCity,Hyogo,676I)023Japan 2}LaboTatory of Insec tScience ,Graduate School ofAgricultural Science ,Kobe Universit y1,-1 Rokkodai-cho ,Nada-ku, Kobe City,Hyogo,657-8501Japan Abstrac tAn ichneumon iwdasp, Melalophachareph 'everese (Uchid ai,957) emerged from the fina linsta rlarva eof a lycaenidbutterfly,Ac),totepispttspa(Horsfield,1828),thathadbeenrearedfromtheeggstageincaptiyLtyinthelaboratory, Thc eggs, oviposited on a leaf of Rosa nfultij7vra, had been collected in a fiel din Tanabe City ,Wiikayama Prefecture. Becausc the wasp cc}uld not have attackcd thc 1ars, aien the laborator ywe, believ ethat the eggs must have been parasitized before they were collected. The ovipositor of M. everese consists of a simple structure lacking the distin cdtorsa lsubapical notch used for attacking active ian'ae ,A!though the biology of spccies with such an ovipositor is poorly known, this structure is strongly associated with hosts that are immobile, Therefore ,we concluded that the paras'ito wiadsp had attacked eggs ofA. puspa. This is the fir srteport suggesting egg-larval developn]en itn M/ eveiese. Key wordsoviposiLor shape, parasito ihdes tstage, ichneumoni wdasp, Campopleginae. Introduction Materials and Methods The ]ycaeni dbutterf iAyc,>'tolqp piusspa (Hersfi eilsd)Seven eggs ot]A, puspa, oviposited on leave sor stems of' found throughout Nansei Shoto and across Kyushu to Rosa m"ltijlora in a bush by the coastal road at Tle aijnzalci southcrn part sof Shikok uand Honshu in Japan ,It is in [[bnab eCity W,akayama Prefectur ew,ere collected on commonincertainlocalitiesandbroodscontinuously,Its November 20, 2010. All of the eggs were kept in a lidded dHiosntsrhiu b, Tuhte irioesn naorwe a fexepawn driencgords toofw paardra tshiet inos romtfhA-,e apsuts pofa pwelraes tr ieccaornetdai niern t(hFe il ag1 b,, o2r0 a×t o1 4r y×w,h 5er,e5 cm )t,h eHya twecrhee d 'lfacr dvRa.e bytheparasitoidwasp,Metatophachampseverese(Uchidam)ulti,flora or M),ric ar"bra from November 2010 to (Hymenopte rIach:neumonidae) ,but the accounts are February 2011. During rearing, six of the seven larsrae partl cyon {1icti anngd the detail hsave been poorl yknown. showed apparent shrinkage in their body size and their The purasito ihdas been observed to emerge f'ro m( 1 ) the body color changed from a shade of green te dark brown, reared prepupae (Kusigem a1t9i67,, 1988) ,(2 )either the Hereafterthe sleaJ'v aaree describ aesd "parasitized larvae". prepupae or the tina linsta lrarva e(Iwat 1a9,91) ,and (3) Leaveswithparasitizedlanfaewereremovedandtransferred pupae reared from the fir sitnsta (rNakan o1 9,94) ,Nakano to another smal] Lidde dplast ibcox (Fi g2., 1O × 7 × 3 cm) supposed tha tthe larv ahad been attacked at the fir sitnstar for observation, The remaining normal 1ary awas fed M. stage, but did not provid eany supporting evidence, nihni unti1 i tdeveloped into an adult blltterfiy. MHCwataseoahs plhnmesa.osprl shoe iotupSps s l iihneaxnora gesJap ciseaihcnipnaae saifoefn mo, ( pworKJhsf mialuceyapvhcseatarieeni s ngeaioaardnveneda mi bokt acabuo1cbetitu9llreni8tsoo8 e,nb)o r gnii.Hfso n o htiwnwthao ithee venetevne h dsebKeo re pyoa,esr urua" as btrhs fhepioaputmrwoo iriel tadysMendd,ent Tdo(HfobeU risHcoodchgrereioningdtpe eaits 1n te,fi9e vhea5yeosrn pe7 ndsae)esv r ,esa(rp se(e2sci dei)tama eo nptiw( saKhd:as=uop:Mm, ta(e owme1tgo )art trhoateefp oe oorhCprfriie hgdttia hnty Macoe, itth h.hd aoTe eflreasbvoocteitrrpsleyiussoppe tw )toe1iaf i.n,ogn Aiewa.vann esdofpu erss uee lgm gaeperbsagtorerad ats thifaotrtr iHoiyze tm.i perttsrhe seh,o fwobeisan tibs apdil elpenycaniserttsaia, 1 sfr tRaiyherte cviw eaaoz sfnetpAtsh. ely ape, suga g sApp4 aa ,sret vraaeegsraeeir setoedfoid xadaRiu ei.tf shv1coc 9ermr5rai 6spi], itp ne oisdatf porheee enafSc is a tmtHjgeheo naeo kmffki eE agmvdiaaeedwlrtoaeee ,b s UrlSynm ahiiKcavnutkeesuerd l r,bsEgnyibeu ti mst KynaaM)uaktus es Cii(negi ue1tbmmy9y,a ,tKt6hai7e n a(a )sng(e3d,acd) wo tnaa(hdt4ea)i puspa. Pref,2,9,ix.2002,I.Wakileg,), ℃orrespondingauthor:my.shima@win,emai1,ne,[email protected] NNIII-IE-leEcltreoncitcronic Library Service TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan 152 M. SIIIMAZAKI et aL s・・-fr"・・・f・,,;,,;.i?・i,t:・,1,:・・c/'l/i't-i'1'tt・}'1,fi.,l/,g . '. .' ' t' :. F. ": ;. . -.tv/,, t ・ ・, 1・ :11' ;,/ll gl,・ii- lii, JlSl-; ;'・'-・ '',・・ gi1s・',/・:ll'i・ Novembeg 20IO 20 10 Janunr y2yell 2eH Fa} Mb) Lc}Ir}eFcMeLmbet; FM LFebruaFrMyL, - 'tx' "y"' LarvaehHtched Slrnmk & dmke ee d Purasito wiadsps on Dec. 1-5 en Jan ,l6- emenged{mjan,22-Feh.I - PIr) eaptu:pean otni oe3nna nJ .a7n. 3 Brnerge coln Feb. 2 a) F: the firs dtecade of a maonth, bj M"nlddle, c) L] ifittes 8 Fig. 1 Containcr used for rearing from cgg stagc. Fig, 2, Box used for the parasiti z1eudrvac. Fig. 3. Ac)'tolep piusspa: a, parasitiz efdina ilnsta !rary ab;, normaL prepupa. Fig ,4, hmerged parasitoi wdasp M, everese. Fig, 5. The shell of the parasiti z1aerdva fror n"'hich M evereTe emerged. Fig. 6. Pupa of A4. ei,eFvse rcmoved from the dead parasiti Llaerdva :a, dorsa laspect: b, Nentral aspect, Fig .7. Female A, puspa. Fig. g. Time course of rcaring, Astereomicroscopc(SZ60,OI:YMPUSCo.,[Ebkyo,Japan; Results1. Mhos1bplgOse6hecO5ritOvm -m,aeiCtncKri,EoosnY c sLowEpeEeNreIC CEaAn Cdt oa( , kCB,elAnOXiM sn4Ewa ieRgtkd hAO,arL ,aa\Jw Ma diCPpinoUag.Sgni,) s tT.,Pa o DmhlCliiooccgtr.yoio,sotg c),waJoreplaarcieppmah anu s sg() oeefadVns dH wtf Xehoare-re A1a nI daIH ne adgttg hsc5e h ,h o2ita0nhte1g cro0h ,f fe[ edii[vgn W tegwo h eaosern frede ta mhagnbei. nafovr aecmrona nlvMti.aat i eiwnereesurrbcr ba o.ef fte tOhwd neRe .le JDmanauenlntcwiuejeiamorrba ye1r, edited using graphi scoftwarc (Adob ePhotoshopO CS3), 20", a grown larv aappeared to have settlcd en a Leaf of R. multij7ora, but it sbody coEer graduall ychanged from a shade of green to dark brown, and it shrunk in size NII-Electronic Library Service TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan Meifalophacha reovep srese attacked eggs of Acytolep pius,spa IS3 'l i ,f・tii・:-:・''gf'ti'i'ii・i'iit'giv・l;lF ・,,, xIX-Ynvg7:={i"df ,,. 11 13 1.e mm (a; )e.5 mm (e,d) Fig.9,FFlegm.ale of M, everese: head. anterior view, Scule bars 1.0 mm. 10.FFiegm.ale of M. everese: mesosoma, ]atera vliew, Scale bars 1.0 mm. Il. FWiingg.s ofM, evereh'e: a, forewin gb;, hindwing, 12.FFiegm.ale of M. evetese: propodeum, dorsa ]view. Seal ebar s1.0 mm. 13, Females of M. everese (a ,b, c) and EribvrMs sp. (d) :a, hind tarsus, later a\[icw; b, metasoma, ]atera] view; c, d, apical par tof ovipositor, later vailews. Arrow shows dorsa slubapical notch. (leng t6 hmmi; width: 3 mm). This abnorma] change was 2. Emergenee qf the ichnettmoni pdarusitoid wasp,fhom laterconfirmedtobeduetoparasitism.Anotherparasititzhee.dfinalinstartarvae 1arv asettled on R, multij7ora and similarly four 1arva ehad On January 22, 2011 a parasito wiasdp oi' the family settled on Ml rubva (Fi g3a.) by January 6, 201 1 , We could Ichneumonidae (Fi g4,) emerged from the fir sptarasitized nuostua ldleyt sepcu ntan byy sai nlokrym aglir pdrle erpouunpda ,a ntdhe a ltl heofr tahxe, psuacrhu sasi tiiszedlofa rtvhea c,asuasmieng s pae csiizeasbl eem eopregneidng i inn dtihev hiodsu t(a flFrlie yg5m .)a n,Woathseprs larva eremained on the leave swithout shedding thei rskin two parasitiz ledarva oen January 24, 20 1 1 . To collect the durin gover the fbllowin gthree weeks. Then the larvae specimens, we placed the box containing the wasps and were transl:er tro etdhe smal 1 ]idde dplast ibcox as described remain ing thre eparasiti zIeadrva ien a refrigerator. When above and observations were continued. Only one 1arva, one ot' the dead parasitiz leadrva ewas cut open, we could osnta glee a(vFe isof g3 M.b,, lruebnrag,t gh1r:0e wmm n;orm awlildyth: t o5 r emamc)h tohne pJraenpuuapray dwiedtthe:c tt2h,e5 dmme)ad ipnuspiad o tefhMe, l aervvera Ae.s efe (maFlie g6A.,, plue.nsgpt abh u:6t mtme;rny 3, 2el1, and shed it sskin to pupate on January 7, 2011, emerged from the unparasitized pupa on February 2, 20 1 1 NNIII-IE-leEcltreoncitcronic Library Service TThhee LLeepipdiopdteorpoltoegircaollSoocgieitycal Society ooff JJaapapnan '154 M.SHIMAZAKI et al, (Fi g7.), The time coursc ef the rearing is given in Fig. 8, been reared from the egg stage in captivity. It is evident which shows that the butter tanldy the parasito iwdasps that the wasp could not have attacked the larva ein the took simitar times to develo apnd emerge. laborator Tyh.ll swe conside[ed tha tthe eggs of A. p",spa had already been attacked by the paraslto {Md. everese 3. Identdicat oiof tnhe parasitoi wdasp when we collected them from the fie[d. The parasitoi wdesre identifi easd M. evetese base don the The time course of rearing (Fi g8.) suggests th at a similar followin gcharacters: ( 1 ) thin and truncate untcrior margin amount of time is rcquircd for the parasito iwadsp and the ofclypeus (Fi g9). ;(2 )scutellum relatively strongly convex lycaeni dlarv ato develop to adults. In addition, there js with apex acutely bent downward jn later avilew; (3 u)pper some observutienal evidence that the pupatio nof the larva h1aOl) fo;(f4 m )fesooprleeuwrionn wgit hcoouvter eadreo wlietth ( tFria ng1s 1v.aer) s;(e r5u g)naeerv el(lFusig. oIfa trhve a palatrhoausgihto wwiaeds pco uwlads cnoomtp lketnedow iwhnesni dtpheue ppaatriaos niwatsized ot'hindwing without angulation (Fi g1 ,1b) ;(6 )propodeum complete, covered with rugae and long silver hairs a,reola and petiolar areas united (Fi g1,2) ;(7 )propodea lspiracle round; (8) The ovipositor of most species ol' Campop[eginue and fir satnd second segments of hind tarsus with 1 ine of robust related subfamiLies (e. gC.remasttnae ,Banchinae and setae on ventral surface, at jrregu ]ianrterva (lFsi g1.3a); Ctenopelmati nhaaes a) dorsa slubapical notch (e. gan.other (9 )fir smettasomtd tergite with glymma and subapica] Campoplegin agecnus Eriborus ,shown in Fig, 13d) ,afld latera lshallow depressio (nFi g1.3b) ;(10 b)erde rbetween this structure may be used to provid esome hold on the tergit eand sternite of firs mtetasomal segment located pierce dintegume noft an active host larva H.owever, the below the mid-hei ght (Fi g1 .3b) ;<1 l) ovipositor short, its ovipositor of M. everese lacks a dorsa lsubapical notch, apex a litt lbeeyond apex of metasoma (Fi g1 .3b) ,without and this condition suggests that it would favo rattacking dorsa lsubapical nQtch <Fig ,13c) ;(12 b)ody co]or black, immovable eggs rather than mobile larvae during secend (foma olre p)osteri poarrt of sccond (mal aend) all oviposition. A similar]y un-notched ovipositor is shown fo11owi ntgergite sreddish brown (Fi g4.); and (13 f)ore in the Stilbopin ageenus Stilbops (Z]wnes 1,970) ,species and mid leg syellowis bhrown cxc1uding coxae, hin dtibia, o(' whieh are known to attack the egg stage of the host and basa lpart of hind basitar spuasrtl ydul lbrown (Fig. (Fitt o1n98,4: S.haw, 1989) .Thus, we suppose that the 4). absence of the notch on the ovipositor is more or less rclated to attacking the hos tat the egg stage. Whilst the usual mode of developme nitn Campop]eginae is larval- Discussion 1arva lt,here 1iav ebeen a couple of reports of egg-larval Campop[eginaearekoinobiontendoparasitoidwasps,mosdtevelopment ,That with most detai i]s a recent study on of whieh attack larva eof Lepidopter a(Towne s1,970), Fl)tposot heorrticol <aGravenho rwhsetre), vari Nouhuys Kusigcmat i( 1 967) was the fir stto report that the parasitoidand Ehmsten (200 4sh)owed that the parasito iovdiposited wasp, Ml everese emerged from a reared prepupa ofA, in larva eshortly prio tro their emergence from the egg. puspa, Among previou sreports, the observations by Iwata The genus Melatophacharop scemprises l'ou rdescribed (1991 a)re almost similar to those present ehdere I,n his specics in the Pa]earct iancd the Orienta rlegions and three report, two of fiv emidd]e-instar larva eofA. puspa did of these species are rcported from Japan (Mi et al., 2005). not reach the prepupa sltage and their body color changed Although several species of ]ycaeni dbutterf lhyave been tdoa drakrek nber hodwons. tl[aIrXvv Mao .e1 e2v edreaseys a ffteerm atlhee s acbmnoerrmgaeld f crhoanmg et.he rtehpeoyi taerde aastt hacoksetd s piecs ineost idberm Mo.n esvterreaste,e d rt.lhb e tshtea gbee astt wohfi ocuhr When he reared another middle-instar larv aofA, p"spa, knowledge, this is the firs treport suggesting that the the larv oaf the parasitoi wdasp grcw to pupat einsid ethe koinobion tendoparasitoid wasp, M. eveiese attacks the host larva and a male M, everese emerged from the egg stage of it shost ,A. p".spa. parasitiz eldarva, Taking these reports together, the wasp has been observed A¢knowledgment to emerge from three dii'f'e rsteangtes of the host: the {inal insta lrarva p,repupa ,and pupa. Howcver. it is uncertain We would lik eto express our cordia[ thanks to Dr Gavin whether this i sdue to dil'ler girnogwth rate ofeach parasitoid Broad (Departm eofn Etntomology ,The Natura lHistory 1arv aor whether the attacking stage of the hos twas different, Museum, London, VK) fbr his review of the manuscript There has been a lac ko'f infOrmati oonn when and how and providin gus with valuable suggestions, the host is parasitiz eHde.re the koinobion etndoparasitoid wasp M, e},eiese ernerged from parasitiz 1eadrva ethat had NII-Electronic Library Service TThhee LLeepipdiopdteorpoltoegiroaollogical SSoooiceityety ooff JJaapapnan ルfelalophacharop esvet’ese attacked eggs ofAc )〜totepi・91,uspa 155 References ル リシジミ卵へ の寄生例 (島暗正美 ・渡辺恭平・島焙 能子) Fit{t〕n, M . G.,1984.Arei・iew ofthe Britis Chol]yrtina, eEucer〔}tina,e Stilbepinae and Neorhacodillae (Hymenoptera : 和歌111県田辺市天神崎海岸沿い 道路傍の野生ノイバ ラに Ichneumonjdae). Ent(丿mt丿1. Gaz.35:185−193. 産卵されてい たヤクシマ ル リシジミの野生卵7個を採取 I wa taσ, Y8た,た皇an99 MLuRsehci〔(}2rd4s3 o)n:3 p7a−r3a8s.i(ltno Ji iadnpsaencets sie)br butterfli(e1s). はし,ノ最イ初バかラら.密5個閉体容に器は内ヤでマ飼モ育モしのた新。葉孵化を与しえたて幼成虫育2個さ体せ Kusige皿lat耄,K.,1967,New HostRecord osflGhneum 〔}nidae from た結果,ノイバ ラ飼育の 正個体に,前師化直前の終令幼虫 Japan. Jns, mats 屍m ,29(2):50, 段階で著しい体長の縮み と体色の黒褐色化を認めた 引き N KSauhks aaiwngbJ,“ oeu’iMmt,e atJ.l匠 e、 ,Rd,9r Kf1(,l97,,1 i9). 9i:e4 S928s a8P93t8a..s .r(AuPlam asna hrjJo,ata3ssopt7i i ratwd(caon1sc ipweo0adT0ss)d p)cfl: coo1hfrn 4Ae 9iS.u−ctn)1o,i tn6loidb0la,eoe(p、pTI ilns piJumahn pf’peaoaエrnJ.ieCaashpee)oafkloelrnemsics 続態しらて寄をき示観生ノ察蜂イしバたがを続た羽ラ飼め化け育,脱てこい出1個れたし体らたと全と。こヤ6引ろ個マ,き体約モ続をモ3き小か飼同さ月育じ後な4寄個密に生体閉最蜂容が初2同器の個様へ個体。 体がのと状移か発 Sc iede echt 〔Hyme 囗Qpにra:Ichneur{n.}nidae, Stilbopin)ae 生した段階で,まだ寄生蜂が出ない個体共々冷凍庫で殺虫 in Scot!and , Entomol. Gaz.40:5−6. 処理 をして寄生蜂を標本にした、,本種はその形態観察か Townes, H, K.,1970. The genera of lchneumonidae, part 3.ルfem. ら.すでにヤクシマ ル リシジミなど6種の シジミチ ョウへ A〃1.ert Enr. lnst.13:1−307. の寄生記録が知られる飼い殺し型内部寄生蜂ツバ メシジミ Uchida, T.,1957. Drei aus den Schmet乳orlillgsl且rven ge乙ucchtete チ ビアメバチMelalolpαhc.’hcu’ops everese (Uchida,1957)だと Iehneumonidenar. tIenns. mats μnt.21:59−61、 回定できた。 今回の採集飼育条件から,ッバ メシジミチビ van Nouhuys, S, andJ . Ehmsten,2004. Wasp behavior leads to アメバチはヤクシマル リシジミの卵に産卵したと考えられ uniform parasしiism of a host available on]y a few hours pef る ツバ メシジミチビアメバ チと同じ亜科や近縁亜科の多 year. Behav. Ecol、15:661−665、 く。の種は寄主幼虫に産卵し,その 産卵管の先端方背面に切 Yu, D. S., K. van Achterberg alld K. Horstman11,2005. World れ込みがあるの に対し,本種は産卵管に切れ込みを欠くの Ichneum{}noidea 2004, Taxonomy, bio;ogy , morphoiogy atlCl で.この産卵管形態は寄主卵に産卵することと関連してい Vdaisntcroiubvuet, krCm、a[nCDaIdDa.VD computcr program]、 Taxapadmp, のる段と考階えでた寄。生こ攻の撃寄を生す蜂るがのシかジはミこチれョまウで成知育ら過れ程てのおいらずずれ, 」L ” 今回の ヤクシマ ル リシジ ミの卵が寄生 されていた とい 摘 要 う知見は初めての記録だと思われる 。 シジミチョウの内部寄生蜂ッバ メシジミチビァメバ チ 〔Recejved Murch 15,201 L Accepted August 26,2011) Melatophαcharops everese (Uchida,1957〕によるヤクシマ 一 NNI工I工-EElleoetcrotniroonic LLiibrbarryary Service