© Entomologica Fennica. 15 February 2016

Notes on Lasioptera rubi (Schrank) (Diptera: ) and its larval () on raspberries in Russia

Ekaterina Yegorenkova & Zoya Yefremova*

Yegorenkova, E. & Yefremova, Z. 2016: Notes on Lasioptera rubi (Schrank) (Diptera: Cecidomyiidae) and its larval parasitoids (Hymenoptera) on rasp-

berries in Russia. — Entomol. Fennica 27: 15—22.

In this paper, larva and of Lasioptera rubi (Schrank) infected by hyme- nopteran parasitoids are illustrated. For the first time it is found that Platygaster pelias Walker is a solitary parasite and winters at the embryonal stage inside host larva ofL. rubi reared from on Rubus idaeus stems in Russia. Lasioptera rubi, Torymus eadyi Graham & Gij swijt and Platygaster pelias Walker are re- corded from Russia for the first time.

E. Yegorenkova, Ulyanovsk State Pedagogical University, Department ofGeog— raplzy andEcology, I 00—letyia Lenina sq., 4, Ulyanovsk 432 700 Russia; E—mail.‘ [email protected] Z. Yefremova, The George S. Wise Faculty ofLife Sciences, Department ofZoo— logy, Tel Aviv University, Tel Aviv 699 78 Israel. * Corresponding author ’s e—mail.‘ [email protected] Received 1 1 June 2015, accepted 3 September 2015

1. Introduction side under the bark of young stems, creating fusiform or irregularly globular swellings. Lar- The raspberry stem midge Lasioptera rubi vae cocoon, pupate and overwinter in the galls on (Schrank, 1803) (Diptera, Cecidomyiidae) oc- the stems ofraspberries and blackberries. In cen- curs from Western Europe to the Far East ofRus- tral Russia, the lengths of gall midge larvae ob- sia and Japan (Yukawa et al. 2014). In Russia, it is served by Batysheva (1982) are equal to 2.0—3.0 widely distributed in the middle and southern mm in 56.3—86.3% ofcases and to 0.7—1.6 mm in parts. It has also been recorded in western Siberia others. (the Yenisei Siberia) (Kolomoets et al. 1989, In Europe, the complex of parasitoids reared Gerasimchuk 2008) and near Krasnoyarsk (Gag- from L. rubi comprises 16 species of Chalcidoi- ne 2004). dea and one species of Platygastridae (Table 1). The damage inflicted on raspberry (Rubus The assemblage includes four species of Apro— idaeus Linnaeus) by galls ofL. rubi (Fig. 1a) in- stocetus and Sigmoplzora brevicornis (Eulo- hibits the growth ofplants and causes partial des- phidae: Tetrastichinae), three species of Eupel— iccation of stems, which may break due to strong mus, Eurytoma and Torymus each, one species of winds. Galls may also reduce crop yields in rasp- Pteromalidae and one of Platygaster (Platy- berry. The raspberry stem gall midge (Fig. 2b) gastridae). can fly for considerable distances (own unpub- Here we illustrate the larval instars ofL. rubi, lished data). The orange-red larvae (Fig. 3c) re- report the development ofits parasitoids, and pro- 16 Yegorenkova & Yefremova ° ENTOMOL. FENNICA Vol. 27

Table 1. Hymenopterous species reared from Lasioptera rubi mines by different authors during 1966— 2006.

Parasitoid family and species Authors Country

Eulophidae roesellae Nees, 1834 Domenichini 1966, Italy, Great Britain, Herting 1978 Russia (Far East of Russia) A. rubi Graham, 1987 Graham 1987, Czechoslovakia (the Jennings 2005 Czech Republic), Finland, France, Germany, Sweden, Yugoslavia (Serbia) A. rubicola Graham, 1987 Graham 1987 Germany A. tymber Walker, 1839 Domenichini 1966, Austria, Czechoslovakia Simova-Tosic & (the Czech Republic), Dobrivojevic 1966, France, Germany, Great Bouek 1977, Britain, Hungary, Viggiani &Mazzone 1978 Netherlands, Sweden

Sigmophora brevicornis (Panzer, 1804) Thompson 1955 Germany, France Eupelmidae Eupelmus fulvipes F'orster, 1860 Boucek 1977, Herting 1978 Yugoslavia (Serbia) E. urozonus Dalman, 1820 Simova-Tosic & Yugoslavia (Serbia) Dobrivojevic1966, Tudor & Neacsu 1983 E. vesicularis (Retzius, 1783) Thompson 1955, Germany, France, Italy, Herting 1978, Viggiani Romania & Mazzone 1978, Tudor & Neacsu 1983

Eurytomidae Eurytoma aterrima (Schrank, 1781) Thompson, 1955 Germany, France E. curculionum Mayr, 1878 Boucek 1977 Yugoslavia (Serbia) E. rosae Nees, 1834 Boucek 1977, Yugoslavia (Serbia), Popescu 2006 Romania Sycophila submutica (Thomson, 1876) Herting 1978 Great Britain

Pteromalidae Mesopolobus rhabdophagae (Graham, 1957) Herting 1978 Great Britain Torymidae Torymus chloromerus (Walker, 1833) Herting 1978, NonNay Stenseth 1978 Torymus eadyi Graham & Gijswijt, 1998 Graham & Gijswijt 1998, Great Britain, Ukraine Popescu 2003, Zerova & Seryogina 2003 T. rubi (Schrank, 1781) Boucek 1977, Yugoslavia (Serbia) Herting 1978 Platygastridae Platygaster pelias Walker, 1836 Vlug 1995 England, Sweden, Spain, Non/vay, Finland, Estonia, Denmark

Vide new ecological and faunistic data on para- 2. Materials and methods sitoids associated with this gall midge. Although Platygaster pelias Walker is well-known as a The study was carried out in June 2009—July parasitoid ofL. rubi, its life history has not been 2010 in two localities of the Ulyanovsk Region: described in details. the Village of Staraya Mayna (68 km E from ENTOMOL. FENNICA Vol. 27 - L. rubi and its larvalparasitoids in Russia 17

e 32.:

Fig. 1. Gall, male and immatures of Lasioptera rubi. — a. Gall on Rubus idaeus (6.6.2009, Ulyanovsk, Russia). — b. Male (reared from a gall). — 0. Third instar larvae (opened gall). — d. Young pupa, dorsal view. — f. Young pupa, ventral view. — f. Mature pupa (ventral view).

Ulyanovsk, 54°36’ N, 48°55’ E) and the city of ting the stems, galls ofL. rubi were placed in plas- Ulyanovsk (the western bank of the river Volga, tic Vials (80X 15 mm) with filter paper and were 54°19’ N, 48°22’ E). Altogether 530 galls ofL. kept in the laboratory at a temperature of +20—22 rubi were collected on raspberries from these 10- OC and shaded from direct sunlight. Selected calities. emergent adults were killed in 75% ethanol for Part ofthe stem, together with a gall, compris- identification. ing 5—7 cm on either side ofthe gall, was cut from A total of 153 galls were dissected to deter- the lower and middle parts ofthe stem. After cut- mine the number of larvae ofL. rubi per gall. The 18 Yegorenkova & Yefremova ° ENTOMOL. FENNICA Vol. 27 remaining 377 galls were kept in containers for land, Sweden, Spain, Norway, Finland, Estonia further rearing: 20% of them became moldy (76 and Denmark (Vlug 1995, Austin et al. 2005, galls), and the rest yielded a total of 582 L. rubi Buhl 2006), and in this study as a new record in adults, 178 specimens of Platygaster pelias Russia. (Proctotrupoidea: Platygastridae), 28 specimens Biology. The species is a larval parasitoid of ofAprostocetus rubi (Chalcidoidea: ) Orthoptera, Hemiptera, Neuroptera, Coleoptera, and 17 specimens of Torymus eadyi (Chalcidoi- Diptera and . Among Cecidomyiidae dea: Torymidae). The parasitoids were identified (Diptera), L. rabi has also been mentioned (Vlug using the keys provided by Trjapitzin (1978), 1995) Storozheva et al. (1995) and Buhl (2006). Platygaster pelias, an egg-larval parasitoid, Voucher specimens are deposited in the Zoologi- has never been mentioned from Russia (Buhl cal Institution of Russian Academy of Sciences 2006). We observed the eggs and larvae ofL. rubi (ZISP), St.-Petersburg, Russia. infected by P. pelias (Fig. 2a). It means that the parasitoids overwinter as embryos. In spring of the following year, the parasitoids develop and 3. Larval and pupal stages emerge in July. Sex ratio (males:females) for ofLasioptem rubi adults of P. pelias reared in laboratory was 182160. A dark yellow-brownish pre—pupa of Dissected galls revealed different numbers of the P. pelias is clearly visible inside the L. rabi larva, raspberry stem gall midge larvae (3—5 larvae in to which it is attached by a filament (Fig. 2b). The 32 cases, 6—8 in 61 cases, 9—11 in 45 cases and stemal spatula ofL. rabi is also visible in ventral 13—14 in 15 cases). Most galls (69%) contained view. The adult of P. pelias breaks through the from6to 11 larvae (average=7.91,S. D. =3.15, n head of the L. rabi larva using its mandibles to = 153). make a hole (Fig. 2c). In all cases there was one The third instar larva ofL. rabi is initially or- P. pelias pupa per prepupal larva of the host that ange-yellow (Fig.1c). At 3.0—3.5 mm length it formed a single parasitoid (Fig. 2b, c). This sug- begins to pupate and young pupa is still orange- gests that only one parasitoid larva develops in yellow dorsally and ventrally (Fig. 1d, e). The each host, and therefore it is a solitary parasitoid. pupa is subsequently turning dark-brown and ma- Several larvae of L. rubi were found with tures (Fig. 1f). P. pelias that had reached the adult stage. So this species of Plalygaster is monembryonic as for example Platygaster matsutama Yoshida & 4. Hymenopteran parasitoids Hirashima that has been reared from Thecodiplo— infecting larvae ofL. rubi sisjaponensis (Diptera: Cecidomyiidae) (Jeon et al. 1985). We establish solitary parasitism of No hymenopterous pupal parasitoids were found P. pelias in L. rubi for the first time. in this study.

4.2. Torymus eadyi Graham & Gijswijt, 4.1. Plagigasterpelias Walker, 1836 1998 (Torymidae) (Platygastridae) Material. The species (Fig. 2f) was represented Material. The species was represented by 178 by 21 specimens: 14?, 38, reared from galls ofL. specimens: 11032, 108, reared from galls of rubi on R. idaeus stems, 15 .VII.2009, Ulyanovsk, L. rubi on stems of R. idaeus 15.7.2009, Ulya- 6.VI.2009 E. N. Yegorenkova leg.; 132, 38, novsk, 6.6.2009 E. N. Yegorenkova leg.; 50?, reared from galls of L. rubi on R. idaeus stems, 88, reared from galls of L. rubi on stems of R. 20.VII.2010, Staraya Mayna, Ulyanovsk provin- idaeus 20.7.2010, Staraya Mayna, Ulyanovsk ce, 14.VI.2010 E. N. Yegorenkova leg. province, 14.VI.2010 E. N. Yegorenkova leg. Comments. The species is distributed in Bul- Comments. This species is distributed in Eng- garia, France, Netherlands, Romania, Ukraine ENTOMOL. FENNICA Vol. 27 - L. rubi and its larvalparasitoids in Russia 19

5%;

Fig. 2. Parasitoids of Lasioptera rubi. — a. Male Platygaster pelias. — b. Pre-pupa P. pelias inside larva of L. rubi (ventral view). — c. Hatching adult of P. pelias (ventral view) from larva of L. rubi (dorsal view). — d. Female Aprostocetus rubi. — e. Pre-pupa of A. rubi (lateral-ventral view) inside larva of L. ani (head of parasitoid larva visible). — f. Female Torymus eadyi.

and England (Graham & Gij swijt 1998, Zerova & Lasioptera rubi has always been mentioned Seryogina 2003), and in this study as a new re- as the only host of T. eadyi (Graham & Gij swijt cord in Russia as it has not been recorded from the 1998, Popescu 2003, Zerova & Seryogina 2003). Middle Volga Region and Russia earlier (Zerova Femalezmale ratio for reared adults was 15 :6. & Seryogina 2003). 20 Yegorenkova & Yefiemova - ENTOMOL. FENNICA Vol. 27

Fig. 3. Details of Apro- stocetus rubi female.

— a. Antenna. — b. Fore-

wing. — c. Ovipositor.

4.3. Aprostocetus rubi Graham, 1987 Propodeum 3.1—3.2 times as broad as long, (Eulophidae) strongly reticulate with median carina, callus with 1 seta. Distance between submedian lines Material. Only females were reared: 28 Q, reared 1.4 times that between submedian and lateral from galls of L. rubi on R. idaeus stems, 10.— lines. Dorsellum 1.25 times as long as propodeum 12.VIII.2009, Ulyanovsk, 6.VI.2009 E. N. Forewing (Fig. 3b): Marginal vein of forewing Yegorenkova leg. with 10—11 setae (10—15 in Graham 1987). Last Other material examined. 132, Germany tergite as long as broad (1.0—1.4 in Graham Baden, Wurttembert, Heilbronn, 3.V.2006 ex 1987). OVipositor sheaths projecting by 0.26 X Lasioptera rubi, K. Schrameyer leg., S. Schmidt length of last tergite (02—05 in Graham 1987). det. 2007. Genitalia (Fig. 3c): outer plates of ovipositor Additions to original description (Graham (T9+T10) 3.1 times as long as broad, 1.3 times as 1987). Female (Fig. 2d) (length 1.3—1.9 mm) long as inner plates ofovipositor, and 3.3 times as (1.8—2.5 mm in Graham 1987). Body black. An- long as ovipositor sheaths. First and second tennae fuscous. Legs yellowish with black coxae. valvulae 1.1 times as long as projecting part of POL (The minimum distance between the poste- sheaths. rior ocelli) 2.0 times as OOL (The minimum dis- Comments. The species is distributed in the tance between the eye margin and the nearest pos- Czech Republic, Finland, France, Germany, terior ocellus). Antenna with 3 anelii (Fig. 3a). Netherlands, Sweden, United Kingdom, Yugo- ENTOMOL. FENNICA Vol. 27 ° L. WM and its larvalparasitoids in Russia 21 slavia (Serbia) (Graham 1987)) and Far East of (eds), Index ofEntomophagous , Vol. 1 : 17101. Le Francois, Paris. 101 pp. Russia (Storozheva et al. 1995, Yefremova 2002) Gagne, R. J. 2004: A catalog ofthe Cecidomyiidae (Dipte- and has been mentioned as a host ofL. rubi (Gra- ra) ofthe world. 7 Memoirs ofthe Entomological So— ham 1987, Jennings 2005) and Diastrophus rubl' ciety of Washington 25: 17108. (Bouché 1834) (Hymenoptera: Cynipidae) Graham, M. W. R. de V. 1987: A reclassification ofthe Eu— (Askew et al. 2006). Aprostocetus rubi has not ropean Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain 7 Bulletin of the been reared from galls in the Middle Volga Re- genera. British Museum (Natural History). Entomology 55(1): it had been collected gion earlier, only by sweep- 173 19. ing (Yegorenkova et al. 2007). In some cases the Graham, M. W. R. de V. & Gijswijt, M. J. 1998: Revision prepupa ofA. rubi may occupy almost 90% ofthe of the European species of Torg/mus Dalman (s. lat.)

7 volume ofthe host body (Fig. 2e). It means that it (Hymenoptera: Torymidae). Zoologische Verhan— delingen, Leiden 317: 88790. is a solitary endoparasitoid. In Fig. 2e, a well-de- Gerasimchuk, A. V. 2008: Phytophagous gall midges veloped head of a parasitoid is adjacent to the (Diptera, Cecidomyiidae) on plants ofsouthern Midd— head of the host larva, whose dark-coloured eyes le Siberia, and their identification by the damage. 7 are clearly visible. In: Baranov, A. A. (ed.), Fauna and ecology zhivotnyh Central Siberia and the Far East. Issue 5: 1327141 State Kras- Acknowledgements. We are grateful to Netta Dorchin (De- Krasnoyarsk Pedagogical University, 298 partment of Zoology, Tel Aviv University, Tel Aviv, Is— noyarsk. pp. [In Russian] B. 1978: A rael) for clarification about the developmental stages ofL. Herting, Neuroptera, Diptera, Siphonaptera. of and ofterrestrial arth- rubi, and to Peter Neerup Buhl (formerly Zoological Mu— catalogue parasites predators Section A. Host or 5. 7 Com— seum, University ofCopenhagen, Denmark) for confirma- ropods. Prey/Enemy, In- tion of P. pelias identification. We thank Naomi Paz (Tel monwealth Agricultural Bureaux, Commonwealth Aviv University) for her help in improving the language of stitute of Biological Control, Ottawa, Ontario, Cana- da. 156 the manuscript. We are also obligated to two anonymous pp. M. T. 2005: rubi Graham, 1987 reviewers for their efforts which greatly improved this pa- Jennings, Aprostocetus new to Britain. 7 per. (Hym., Eulophidae) Entomologist’s Monthly Magazine 141(1694/ 1696): 150. Jeon, M. J., Lee, B. Y. & K0, J. H. 1985: Ecology ofPlaly- gaster matsutama and Inostemma seoulis (Hymenop— References tera: Platygastridae), egg-larval parasites of the pine needle gall midge, Thecodiplosisjaponensis (Diptera, Cecidomyiidae). 7 Esakia 23: 1317143. R. J. N. Askew, R., Plantard, 0., Gomez, F., Hernandez, Kolomoets, T. P., Mamaev, B. M., Zerova, M. D., Nar- M. & J. L. 2006: of Nieves—Aldrey, Catalogue parasi— chuk, E. P., Ermolenko, V. M. & Dyakonchuk, M. A. toids and in of inquilines galls Aylacini, Diplolepini 1989: Nasekomye—galloobrazovateli kul’turnyh i di— and in West Palaearc- Pediaspidini (Hym., Cynipidae) korastushih rasteniy evropeyskoy chasti SSSR. Dvuk— tic. 7 Zootaxa 1301: 3760. rylye [Gall-forming insects of cultivated and wild

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