ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN

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1 REDIA, LXXXIX, 2006: HOSSEINALI LOTFALIZADEH (*) - JEAN-YVES RASPLUS (**) - GÉRARD DELVARE (**) ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN (*) Department of Insect Taxonomy, Iranian Research Institute of Plant Protection, P. O. B , Tehran, Iran; hlotfalizadeh2001@yahoo.com (**) UMR INRA CIRAD IRD AGROM. Centre de Biologie et de Gestion des Populations (CBGP), Campus International de Baillarguet, Montpellier Cedex 5, France Lotfalizadeh H., Rasplus J.-Y., Delvare G. Rose gall wasps and their associated fauna (Hymenoptera) in Iran. Over a four year period, the rose gall wasps (Diplolepis spp.) and their associated fauna were studied in the northern regions of Iran. Seventeen species of parasitic wasps were collected and identified, eleven of them are recorded for the first time from Iran. They belong to two superfamilies: Chalcidoidea (16 species belonging to 5 families) and Ichneumonoidea (one ichneumonid species). Eurytoma collina Zerova, 1977 is newly transferred to the genus Aximopsis (comb. n.). A brief biological review of the parasitoids associated with cynipids wasps is given. This complex was compared to those reported in some others countries. A review (Table) of the previous citations of parasitoids associated with Diplolepis species on Rosa sp. in the West-Palearctic is given. A key to the species occurring in Iran is given and illustrated to enable ecologists to better identify the wasps associated with Diplolepis galls. KEY WORDS: Cynipidae, parasitoids, Chalcidoidea, Rosa, fauna, Iran. INTRODUCTION Species of Rosa are one of the main ornamental plants. Among them, the Dog rose (Rosa canina L.), as a wild ancestral rose, is commonly used in Iran as stock for scion of other cultivated roses. Another species, the Damask rose 1 (Rosa damascena Mill.) grows well in semi-arid areas in Iran (e.g. Kashan) and has a locally strong economic value as it is used to make several products (such as rose water and rose oil) that are largely used in food technology. Among the bioagressors of Rosa species, the cynipid gall wasps of the genus Diplolepis Geoffroy (Rose gall wasps) (Hymenoptera: Cynipidae) can do great damage to many cultivated and wild rose species. SCHRÖDER (1967) believed that rose gall wasp was one of the most promising insects for the biological control of sweet brier (Rosa rubiginosa L.) in New Zealand. Diplolepis (=Rhodites) is one of the most widely distributed genus of family Cynipidae (VYRZHIKOVSKAJA, 1963). It occurs in a great variety of ecological sites, from the sea shore to the high mountains (SCHRÖDER, 1967). The taxonomy and phylogeny of the genus Diplolepis was recently investigated (PUJADE I VILLAR, 1993; PLANTARD et al., 1998). PUJADE I VILLAR & PLANTARD (2001) especially studied the Diplolepis rosae complex. The ecological and economic importance of Rose gall wasps induced a number of studies concerning the large community of parasitoids which attacks the Rose gall wasps (ASKEW, 1960; SCHRÖDER, 1967; NORDLANDER, 1973; ZEROVA & D YAKONCHUK, 1976; NIEVES ALDREY, 1981 and SHORTHOUSE, 1993). Nevertheless up to now no such studies have been done in Iran. Recently, RAKHSHANI et al. (2003) reported several parasitoids of Diplolepis sp. on dog rose at Tehran but they did not provide any biological information. While this manuscript was prepared a paper was published (ASKEW et al., 2006) reporting the Chalcidoidea reared on Diplolepis mayri (Schlechtehdal) in Iran. About 45 species of 1 Monthly rose or Persian rose. parasitoids belonging to 18 genera are known to be associated with Diplolepis species on Rosa sp. in the Palaearctic region (ASKEW, 1960; SCHRÖDER, 1967; NORDLANDER, 1973; ZEROVA & D YAKONCHUK, 1976; NIEVES ALDREY, 1981 and NOYES, 2002) (Table 1). Similarly, SHORTHOUSE (1973) reported four species from the Nearctic region. The purposes of this paper are: 1) Review the associated parasitoids of rose gall wasps in Iran; 2) Study the fauna associated with Diplolepis fructuum (Rübsaamen, 1882), as only one species was previously reported (ZEROVA & SEREGINA, 1992); 3) Provide new hosts and distributional records for some species and 4) Compare the community in Iran with that found in other countries. MATERIALS AND METHODS Over a four year period (1996, 2002, 2003 and 2005), between April and August, observations were made at the different Agricultural Research field stations in Iran. The Diplolepis galls on Dog rose (Rosa canina L.) and Damask rose (Rosa damascena Mill.) were collected in three field stations at Azarbaijan-e-Sharghi Province (East- Azarbaijan): 1- Peyam/Yam (38 21 N, E); 2- Marand (38 25 N, E); 3- Zonuz (38 35 N, E) and finally 4- Tehran, Evin (35 47 N, E) in 2002 (fig. I). Both fresh (immature) and dry (mature) galls were collected. The galls were kept separately in transparent plastic containers and under room conditions until the parasitoids emerged. The containers were checked every day and recently emerged parasitoids removed. Parasitoids were subsequently killed in alcohol. All reared specimens were card-mounted based on NOYES (1982). Reared wasp specimens were determined by using the following works or revisions: KIERYCH (1966), GRAHAM (1969), BOUČEK (1970), GAULD & MITCHELL (1977), GRAHAM (1987); BOUČEK & RASPLUS (1991), PUJADE I VILLAR (1993), GIBSON, (1995), GRISSELL (1995), ZEROVA (1995), Received 28 November 2006 Accepted 3 May 2007 Published June 2007

2 74 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX Table 1 Associated fauna of Diplolepis spp. on Rosa spp. in the Palaearctic Region from ZEROVA & D YAKONCHUK (1976), PLANTARD (1996), NOYES (2002) and ASKEW et al. (2006). Parasitoids species Diplolepis species Parasitoids species Diplolepis species Cynipidae Periclistus brandtii (Ratzeburg, 1832) rosae, mayri P. caninae (Hartig, 1840) centifoliae P. Dettmer, 1924 Eulophidae Aprostocetus aurantiacus (Ratzeburg, 1852) eglanteriae, mayri, nervosa,, centifoliae A. eurytomae (Nees, 1834) nervosa, eglanteriae, centifoliae, mayri, Aprostocetus sp. Baryscapus pallidae Graham, 1991 Aulogymnus skianeuros (Ratzeburg, 1844) Minotetrastichus frontalis (Nees, 1834) Pediobius sp. (nr saulius) Eupelmidae Eupelmus atropurpureus Dalman, 1820 mayri mayri rosae rosae mayri, centifoliae E. muellneri Ruschka, 1921 mayri E. urozonus Dalman, 1820 mayri, rosae, eglanteriae, centifoliae E. vesicularis (Retzius, 1783) mayri, rosae,, centifoliae Eurytomidae Aximopsis collina (Zerova, 1984) sp. E. cynipicola Zerova, 1976 mayri, magna E. nikolskayae Zerova, 1989 mayri E. parvula Thomson, 1876 rosae «E.» pistaciae Rondani, 1877 mayri Eurytoma rosae Nees, 1834 mayri, nervosa, rosae, rosarum, eglanteriae, centifoliae, Sycophila biguttata (Swederus, 1795) rosae S. variegata (Curtis, 1831) sp. Ichneumonidae Orthopelma brevicorne Morley, 1907 eglanteriae, O. mediator (Thunberg, 1882) rosae, mayri,, centifoliae Ormyridae Ormyrus nitidulus (Fabricius,1804) Pteromalidae Caenacis inflexa (Ratzeburg, 1848) Hobbya stenonota (Ratzeburg, 1848) Pteromalus bedeguaris (Linnaeus, 1758) Mesopolobus amaenus (Walker, 1834) Mesopolobus sericeus (Forster, 1770) Spaniopus dissimilis Walker, 1833 rosae rosae, mayri, mayri nervosa, rosae, rosarum, eglanteriae, mayri, centifoliae, mayri mayri, rosae rosae Torymidae Glyphomerus carinatus Nikol skaya, 1952 spinosa, Glyphomerus stigma (Fabricius, 1793) rosae, eglanteriae, centifoliae,, mayri Glyphomerus tibialis Förster, 1856, centifoliae Monodontomerus aereus Walker, 1834 rosae Pseudotorymus regalis Askew, 2006 mayri Pseudotorymus rosarum (Zerova & Seregina, 1992) fructuum P. sapphyrinus (Fonscolombe, 1832) rosae Torymus angelicae (Walker, 1836) rosae T. bedeguaris (Linnaeus, 1758) rosae, spinosa, mayri, polita, centifoliae, T. chloromerus (Walker, 1833) mayri, rosae, centifoliae, spinosa T. eglanteriae Mayr, 1874 mayri, eglanteriae, T. flavipes (Walker, 1833) rosae, mayri, spinosa T. laetus (Walker, 1833) eglanteriae T. macropterus (Walker, 1833) rosae, mayri, spinosa T. microstigma (Walker, 1833) eglanteriae T. montanus Zerova, 1976 mayri, rosae T. rubi (Schrank, 1781) rosae, spinosa, mayri,, centifoliae T. scutellaris (Walker, 1833) rosae GIBSON et al. (1997), GRAHAM & GIJSWIJT (1998), ZEROVA & SEREGINA (1999) and ASKEW & NIEVES ALDREY (2000). Here we list the species occurring in studied field stations in northern parts of Iran. A simple identification key is provided to the species that were collected during this investigation. Finally, the composition of the associated complex is compared with those of the other temperate regions. For all the parasitoid species information is given on host, distribution, diagnostic characters and preliminary biological data. RESULTS AND DISCUSSION All the parasitoids reared in this survey belong to two superfamilies of Hymenoptera: Chalcidoidea and Ichneumonoidea. Five families of chalcid wasps are represented: Eulophidae, Eupelmidae, Eurytomidae, Pteromalidae and Torymidae. The family Ormyridae was not observed during this research, although it is known to occur in Diplolepis galls. Only one species of Ichneumonidae, Orthopelma mediator (Thunberg, 1882), was reared from rose galls. We did not investigate the trophic relationships of the complex within the galls but, according to HERTING (1976, 1977) and BOUČEK, & ASKEW (1968) Aprostocetus eurytomae (Nees, 1834), Eupelmus urozonus Dalman, 1820, Torymus bedeguaris (L., 1758) and Pteromalus bedeguaris (L., 1758) may be hyperparasitoids. PLANTARD (1996) divided the parasitoid community associated with Diplolepis Giraud according to the trophic relationships; this author pointed out four groups: 1- Phytophagous species (such as Periclistus ), 2- Primary parasitoids (such as O. mediator, A. eurytomae and G. tibialis Förster, 1856), 3- Facultative hyperparasitoids that attack Diplolepis and Periclistus Foerster [Pteromalus bedeguaris, Glyphomerus stigma (Fab., 1793), Eupelmus atropurpureus Dalman, 1820 and Eupelmus vesicularis (Retzius, 1783)], 4- Exclusive parasitoids (Eurytoma rosae Nees, 1834). In a recent sample reared in 2005 from fruit galls on

3 Anno 2006 ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN 75 Fig. I Map of Iran with collection localities of studied specimens. R. canina, eight phenological groups were identified that emerged in spring from D. fructuum galls (with some overlapping): 1- Orthopelma mediator (April); 2- Pteromalus bedeguaris (April); 3- Eupelmus urozonus (April-June); 4-Aprostocetus eurytomae (April-June); 5- Torymus bedeguaris (June); 6- Eurytoma rosae and Eurytoma caninae Lotfalizadeh & Delvare, 2007 (June); 7- Aximopsis collina, «Eurytoma» sp.1 and «Eurytoma» sp.3 (June); 8- Glyphomerus stigma (June-July). P. bedeguaris and E. caninae were the last parasitoids observed in June and July. The sequence of these emerging periods is similar to that found from galls of D. in France (PLANTARD, 1996). Species belonging to Eulophidae, Pteromalidae and Torymidae are predominant among the parasitoids of D. fructuum, constituting approximately 80% of their number. The species associated with D. fructuum in the present study form a rich community (17 species). The species richness from Iran is even greater than that reported in Europe (Table 3). Conversely the complex associated with another Rose gall wasp [which might be D. nervosa (Curtis)] included only six species (Table 2). Further investigations especially from other parts of the country (southern and eastern areas) are of course needed to complete this preliminary information. Cynipidae We collected respectively fruit and leaf galls. The cynipid wasp galling fruit is identified as Diplolepis fructuum. No Diplolepis adults emerged from the galls collected on the Damask rose (Rosa damascena Mill.) but according to the shape of the galls, the gall inducer should be Diplolepis nervosa (Curtis). Six parasitoids emerged from leaf galls: Pteromalus bedeguaris, Eurytoma rosae, Eurytoma caninae, Eupelmus urozonus, Eupelmus fulvipes and Caenacis inflexa (Table 2). ASKEW et al. (2006) in the recent study recorded D. mayri from Iran. Table 2 List of parasitoids associated with rose galls in northern part of Iran. Parasitoids Rosa galls Diplolepis Diplolepis fructuum nervosa Aprostocetus eurytomae + - Aprostocetus aurantiacus + - Eupelmus urozonus + + Eupelmus fulvipes - + Aximopsis collina + - Eurytoma caninae + + Eurytoma rosae + + «Eurytoma» sp «Eurytoma» sp «Eurytoma» sp Sycophila biguttata + - Orthopelma mediator + - Caenacis inflexa - + Pteromalus bedeguaris + + Glyphomerus stigma + - Torymus bedeguaris + - Torymus auratus + - Diplolepis fructuum (Rübsaamen, 1882) Material examined Azarbaijan-e-Shraghi, Peyam, 25.iii.2002, 5.v.2002, 22.iv.2005, ex galls on Rosa canina (H. Lotfalizadeh), 72. Tehran, Evin, 6.vi.2002, ex galls on Rosa canina, (H. Lotfalizadeh), 18. Notes This gall-maker on fruit of Rosa canina was collected in a large numbers in North of Iran but from female sex only. Otherwise it was collected from Iran (by Gholdansaz) (PLANTARD et al., 1998), Turkey (PUJADE I VILLAR & PLANTARD, 2001) and former USSR (ZEROVA & D YAKONCHUK, 1976).

4 76 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX Table 3 Comparative list of rose gall associated wasps in different countries. Iran France UK Former USSR Europe (1) Parasitoids D. fructuum D. D. rosae D. mayri D. rosae Aprostocetus eurytomae + + Aprostocetus aurantiacus + Eupelmus urozonus Eupelmus fulvipes + Eupelmus atropurpureus + Eupelmus muellneri + Eupelmus vesicularis + Aximopsis collina + Eurytoma caninae + + (2) Eurytoma cynipicola + Eurytoma rosae «Eurytoma» pistaciae + (3) «Eurytoma» sp.1 + «Eurytoma» sp.2 + «Eurytoma» sp.3 + Sycophila biguttata + + Orthopelma mediator Orthopelma brevicornis Caenacis inflexa Pteromalus bedeguaris Spaniopus dissimilis + Mesopolobus sericeus + Glyphomerus carinatus + Glyphomerus stigma Torymus auratus + Torymus bedeguaris Torymus chloromerus + Torymus eglanteriae Torymus macropterus + + Torymus montanus + Torymus vesicularis + References PLANTARD (1996) ASKEW (1960) ZEROVA & SCHRÖDER (1967) D YAKONCHUK (1976) 1 Reported from: Spain, France, Switzerland, Germany, Austria and Slovakia. 2 Reported by LOTFALIZADEH et al. (2007a). 3 Reported as Eurytoma setigera which was synonymized with E. pistaciae by BOUČEK (1974); nevertheless trecent examination of reared specimens seem to show that E. setigera is a valid species. Morphologically the species is quite similar to Diplolepis rosae and Diplolepis mayri (Schlechtendal) and most easily confused with them. Nevertheless KIERYCH (1966) identified it through several characters: scutellum sharply constricted apically, with distinct apical projection (fig. II, 2), propodeum without carinae, closed radial cell on forewing (fig. II, 1) and large areola. ZEROVA & D YAKONCHUK (1976) hypothesized that D. fructuum was simply a southern population and therefore a synonym of D. mayri. Conversely, PLANTARD et al. (1998), based on a molecular study, confirmed the validity of this species. Recently PUJADE I VILLAR & PLANTARD (2001) compared this species with three species of the rosae-complex (D. rosae, D. mayri and D. ). From molecular and morphological evidence they considered D. fructuum a valid species. The species also differs biologically: it induces galls on fruits instead of buds. The galls may be recognised by their size and shape and are plurilocular; the external wall is not covered by branching hairs but is smooth or with some short spines as in D. mayri. Eulophidae ASKEW et al. (2006) reported Baryscapus pallidae Graham and a single specimen of an unknown species of Pediobius (near to saulius) but in our study two species belonging to the genus Aprostocetus (Tetrastichinae) were recorded: Aprostocetus aurantiacus (Ratzeburg, 1848) Material examined Azarbaijan-e-Shraghi, Peyam, 6.vi.2002, ex D. fructuum on R. canina, (H. Lotfalizadeh), 20 & 4. Same data, 29.iv.2005, 31 & 13. Tehran, Evin, 6.vi.2002, D. fructuum on R. canina, (H. Lotfalizadeh), 15. Notes This endoparasitoid of Diplolepis species was frequently collected on Diplolepis fructuum. It was previously recorded from western parts of Europe (NOYES, 2002) but is new to Iran. A. aurantiacus is morphologically closely related to A. eurytomae. Its female differs mostly by the funicular segments subequal in length or decreasing very slightly, the gaster shorter and ovate, the last abdominal tergite slightly shorter than its basal breath, and the ovipositor sheaths very slightly exerted (fig. III, 2). Aprostocetus eurytomae (Nees, 1834) Material examined Azarbaijan-e-Shraghi, Peyam, 5.v.2002, ex Diplolepis fructuum on R. canina, (H. Lotfalizadeh), 4 & 1. Same data, 12.ix.2003, 2. Same data, 29.iv.2005, 19 & 8. Zonuz, ex D. fructuum on R. canina, vii.1996, (H. Lotfalizadeh), 2. Notes Our samples include the two described forms of

5 Anno 2006 ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN 77 Fig. II Diplolepis fructuum: 1. Female profile in lateral view; 2. Mesoscutum and scutellum in dorsal view. Orthopelma mediator: 3. Pro - podeum; 4. Female profile in lateral view; 5. Male profile in lateral view. A. eurytomae quoted by GRAHAM (1987). Most specimens collected from Peyam belong to the darker form but 2 specimens collected from Zonuz have a completely pale pedicel while their funicular segments are brown and the ovipositor sheaths brown to dark distally. Iranian population of A. eurytomae seems morphologically intermediate between the populations inhabiting northern and southern Europe. The Iranian specimens are similar to the darker forms described by GRAHAM (1987), but the dorsellum is completely black, tarsi testaceous black distally, tegulae testaceous. The species was classified in the auranticus-group of the subgenus Aprostocetus by GRAHAM (1987). The same author mentioned that Tetrastichus avellanae Kostjukov, 1978 which was recorded from Armenia could just be a darker form of A. eurytomae. In this species the funicular segments are longer than wide, the gaster longer than head plus mesosoma, the last abdominal tergite times as long as broad, and the ovipositor sheath distinctly exerted (fig. III, 3). It is a gregarious parasitoid in galls of several species of Diplolepis in the Palaearctic region. This new record on D. fructuum is also the first for Iran. Eupelmidae Two species of Eupelmus emerged from Diplolepis galls in our sample: Eupelmus urozonus and Eupelmus fulvipes; they both belong to the urozonus species-group. The other recorded species in this family are Eupelmus (Macroneura) muellneri Ruschka, 1921 (ZEROVA & D YAKONCHUK, 1976), reported from D. mayri, E. (Macroneura) vesicularis and E. atropurpureus Dalman (PLANTARD, 1996). All of them (females only) are mostly brachypterous species that can be easily distinguished. Eupelmus urozonus Dalman, 1820 Material examined Azarbaijan-e-Shraghi, Peyam, 5.v.2002, ex D. fructuum on R. canina, (H. Lotfalizadeh), 6. Same data, 18.v.2002, 8 & 2. Same data, 12.ix.2003, 3 & 2. Azarbaijan-e-Shraghi, Marand, 17.viii.2003, ex leaf-gall on Rosa damascena, (H. Lotfalizadeh), 4. Tehran, Evin, 6.vi.2002, D. fructuum on R. canina, (H. Lotfalizadeh), 11.

6 78 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX Fig. III Aprostocetus aurantiacus: 1. Female habitus in dorsal view; 2. The last gastral segments and ovipositor. Aprostocetus eurytomae: 3. last gastral segments and ovipositor. Eupelmus urozonus: 4. Female profile in lateral view; 5. Mid tarsi; 6. Head and mesosoma in lateral view; 7. Male antenna. Notes The species is supposed to exhibit a broad host range species including sawflies, cynipids, butterflies and moths, flies and beetles: 112 species are quoted by NOYES (2002). Nevertheless we are already able to recognize from fine but distinct morphological characters at least six different forms which are presently identified as E. urozonus according to the available keys (GIBSON, 1995; ASKEW & NIEVES ALDREY, 2000). These forms are also segregated according to different hosts. This shows that under this name a complex of sibling species is most probably present. Further morphological and molecular data are badly needed to separate the actual species belonging to this complex and to infer their relationships. This common species is supposedly widely distributed from Australasia to, Europe, and even North America (SCHRÖDER, 1967; NOYES, 2002). It has long marginal vein (4 times length of postmarginal vein) (fig. III, 4), meso-basitarsus with more than twenty dark pegs ventrally (fig. III, 5), ovipositor with basal white band. Male antenna is as fig. III, 7. Eupelmus fulvipes Förster, 1860 Material examined Azarbaijan-e-Shraghi, Zonuz, ex. leafgall on Rosa damascena, vii.1996, (H. Lotfalizadeh), 1. Same data, vii.2002, 2 & 5. Notes E. fulvipes is similar to E. urozonus but may be recognized by its almost entirely pale femora and tibiae and its postmarginal vein slightly longer than stigmal vein. Furthermore males of E. fulvipes are characterized by the presence of a carina on the vertex. It is widely distributed in the West-Palaeactic region (NOYES, 2002) but is a new record for Iran. This species was previously recorded as a parasitoid of Aporia crataegi (L., 1758) (Lep.: Pieridae) and Lasioptera rubi (Schrank, 1803) (Dip.: Cecidomyidae) on Rubus idaeus (HERTING, 1976). It was reared in France on Rosa spp. (PLANTARD, 1996) and this biology is confirmed here.

7 Anno 2006 ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN 79 Eurytomidae Three genera, Eurytoma (5 species in 2 species-groups), Aximopsis (one species belonging to the nodularis speciesgroup) and Sycophila (one species) associated with Diplolepis were collected. The status of three unnamed species of Eurytoma needs more material and further type comparison to be assessed correctly. Therefore these species are not described here. Aximopsis collina (Zerova, 1977) comb. n. ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 8, 1. Tehran, Evin, ex D. fructuum on R. canina, 11.viii.2002, (H. Lotfalizadeh), 2, 5. Notes A recent phylogenetic study on the subfamily Eurytominae (LOTFALIZADEH et al., 2007b) showed that the genus Eurytoma as traditionally understood, e. g. with sharp genal edge, was clearly a polyphyletic assemblage. These authors redefined the genus in a much narrower concept. Following this the nodularis species-group of authors was included in the genus Aximopsis Ashmead here defined in a broader sense. The new combination proposed is just a consequence of the above results. In Aximopsis the mesopleuron exhibits a conspicuous ventral shelf (fig. IV, 4), carinate fore coxae (fig. V, 1) and the female gaster is distinctly petiolate. A male antennal segment is as fig. V, 2. A. collina was found abundantly in Azarbaijan-e-Sharghi Province and Tehran. This species was originally reared from an unknown Diplolepis species and the association with D. fructuum is a new record. The type material was collected in Uzbekistan; the species was also reported from Tadzhikistan and Turkmenistan (NOYES, 2002). It is newly recorded in Iran. Eurytoma caninae Lotfalizadeh, Delvare & Rasplus, 2007 Material examined Paratypes; Azarbaijan-e-Sharghi Province, Peyam, ex D. fructuum on R. canina, 15.iv.2005, (H. Lotfalizadeh), 17 & 8. Tehran, Agasht, ex Diplolepis sp. on R. canina, v.2003, (E. Rakhshani), 10 & 9. Fig. IV Sycophila bigattata: 1. Forewing. «Eurytoma» pistaciae: 2. Hind leg in lateral view. Eurytoma rosae: 3. Female profile in lateral view; 7. Forewing venation. Aximopsis collina: 4. Head and mesosoma in lateral view; 6. Forewing venation. Eurytoma caninae:5. Head and mesosoma in lateral view.

8 80 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX Notes This recently described species belongs to the rosae species-group (LOTFALIZADEH et al., 2007b). It was studied from morphological and molecular aspects and compared with Eurytoma rosae itself (LOTFALIZADEH et al., 2007a). The species is quite common but was previously overlooked with E. rosae, most probably because the adults of both species emerge synchronously from the same galls of Diplolepis. It can be distinguished by different characters: clypeus very slightly emarginate (slightly bilobed in E. rosae), lower face mostly strigose (punctured with short striate near oral fossa in E. rosae), median furrow of propodeum not delimited laterally (delimited in E. rosae), mid coxae without lamella (figs. IV, 5 and V, 4) (with distinct lamella (fig. V, 5) in E. rosae). Eurytoma rosae Nees, 1834 ex D. fructuum on R. canina, 5& 18.v.2002, (H. Lotfalizadeh), 2 & 2. Same data, 12.ix.2003, 7 & 2. Azarbaijan-e- Sharghi Province, Zonuz, ex leaf-gall on R. damascena, 11.viii.2002, (H. Lotfalizadeh), 1 & 1. Azarbaijan-e- Sharghi Province, Marand, ex. leaf-gall on Rosa damascena, 17.viii.2002, (H. Lotfalizadeh), 2. Tehran, Evin, ex D. fructuum on R. canina, 11.viii.2002, (H. Lotfalizadeh), 4. Tehran, ex Diplolepis sp. on R. canina, 2003, (E. Rakhshani), 3 & 2. Notes The species is a common parasitoid of Diplolepis that was reared on galls of R. canina and R. damascena, in Iran. The specimens reared from leaf-galls on R. damascena are smaller than those found in fruit-galls of R. canina. It is largely distributed in the Holarctics (NOYES, 2002) and was reported from Iran as a parasitoid in galls of an unknown Diplolepis (RAKHSHANI et al., 2003). CLARIDGE & ASKEW (1960) confirmed Blair s observation (1944, 1945) and showed that the larvae of E. rosae feed on the gall tissue. ZEROVA & D YAKONCHUK (1976) quoted this species as ectoparasitic on the larvae of D. mayri. Male antennal segments as fig. V, 3. «Eurytoma» sp.1 ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 2. Same data, 12.ix.2003, 3. Same data, 29.v.2005, 2 & 1. Zonuz, ex D. fructuum on R. canina, vii.1996, (H. Lotfalizadeh), 1. Notes This species, and the two following species of Eurytoma, undoubted represent undescribed species belonging to the pistaciae-dentata species-group. They could not belong to genus Eurytoma, because in this group the postgenal lamina is not raised ventrally over the surface of the postgena (in Eurytoma s. s. raised ventrally over the surface of the postgena, therefore visible as a tooth in lateral view); in addition postgena has no a ventral depression between the posterior margin of the gena and the hypostomal fossa (LOTFALIZADEH et al., 2007b). It is awaiting generic placement. This distinct group can be determined by the following characters: clypeus bilobed, lower face punctured, supraclypeal area smooth, antennal toruli with raised inner margins, intertorular space sulcate, notauli superficial, prepectus with subventral carinae enclosing a trapezoidal areola, transverse petiole bearing basolateral teeth and delimited from first gastral sternite by a ridge. Also in E. pistaciae and related species (such as «E.» sp.1, «E.» sp.2 and «E.» sp.3), the metatibiae bear large spiniform setae at their bases (fig. IV, 2) (DOǦANLAR & ÇAM, 1991). We do not wish to describe the new species at present because of insufficient material. «E.» sp.1 is well separated from the two other undescribed species of Eurytoma by the superficial and step-like notauli; scape brownish-black, slightly swollen distally. «Eurytoma» sp. 2 ex D. fructuum on R. canina, 12.ix.2003, (H. Lotfalizadeh), 1. Tehran, ex Diplolepis sp. on R. canina, 2003, (E. Rakhshani), 1. Notes This species has deep and groove-like notauli, scape distinctly swollen distally, propodeum finely reticulate medially, scutellum with large piliferous punctuation (frontal margin of scutellum (behind transscutal line) with 3 or less than 3 punctures. Also, the gaster in this species was longer than in the others and 4 th tergite covered partially 5 th tergite (in the others it is covered completely), nevertheless we did not consider this character as a key character because these materials were conserved in ethanol and the gaster may have been deformed. «Eurytoma» sp. 3 Material examined Azarbaijan-e-Sharghi Province, Zonuz, ex. leaf-gall on R. damascena, 11.viii.2002, (H. Lotfalizadeh), 1. Tehran, ex Diplolepis sp. on R. canina, 2003, (E. Rakhshani), 3. Notes This species has deep and groove-like notauli (such as «E.» sp.2) but scape and propodeum are the same as «E.» sp.1 Sycophila biguttata (Swederus, 1795) ex D. fructuum on R. canina, 6.v.2002, (H. Lotfalizadeh), 1. Notes The species was rarely reared on dog rose in Peyam area and was recently collected on cynipid galls of Quercus in different regions of Iran (Ilam Province by B. Gharali and E. Azizkhani in Lorestan Province). It was reared by ZEROVA & D YAKONCHUK (1976) on D. mayri. It is a common parasitoid of many genera of cynipid wasps on Quercus such as: Andricus, Biorhiza, Cynips, Neuroterus (PUJADE I VILLAR, 1994; NOYES, 2002). D. fructuum is a new host for this species. The genus, Sycophila have a distinct submarginal infumation (fig. IV, 1), antennae has same profile in the two sexes except that the males have a 4-segmented and females a 5-segmented funicle, long abdominal petiole in both sexes, basal submedian carina of propodeum forming inverted V- shape, thickened marginal vein, distinctly bilobed clypeus, several bristle-like hairs on dorsal side of hind tibiae. Sycophila biguttata as a widespread species in the Palaearctic region can be differentiated from Sycophila variegata (Curtis) which was also collected in association with rose galls (ZEROVA, 1995) by its longer marginal vein (four times as long as wide), the stigmal vein shorter than the marginal vein and the 3-8 stout spines which are as wide as hind tibia (not longer than hind tibia in distal part). Pteromalidae Two pteromalid species; Pteromalus bedeguaris and Caenacis inflexa were collected on Rosa. Two other Ptero -

9 Anno 2006 ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN 81 malidae are associated with the rose galls: Mesopolobus sericeus (Förster) in Europe and Spaniopus dissimilis Walker in Europe and USA (HERTING, 1977). In addition, single specimens of Hobbya stenonota (Ratzeburg) and Mesopolobus amaenus (Walker) were recorded on D. mayri in Iran (ASKEW et al., 2006). Pteromalus bedeguaris Thomson, 1878 ex D. fructuum on R. canina, 18.v.2002, (H. Lotfalizadeh), 24 & 10. Same data, 12.ix.2003, 19 & 5. Same data, 30.iv.2005, 14 & 11. Azarbaijan-e-Sharghi Province, Zonuz, ex. leaf-gall on Rosa damascena, 11.viii.2002, (H. Lotfalizadeh), 2 & 3. Tehran, Evin, ex D. fructuum on R. canina, 11.viii.2002, (H. Lotfalizadeh), 18 & 10. Notes According to our observation, the species emerges in large numbers from D. fructuum galls, representing approximately 40 % of the total number of parasitoids. It is a common ectoparasitoid of larvae of Diplolepis species on Rosa (Table 1). The species was also recorded as an hyperparasitoid of Glyphomerus stigma, Orthopelma mediator, Periclistus brandtii, Torymus bedeguaris (NOYES, 2002). P. bedeguaris can been identified by the following characters: anterior margin and distal third of the basal cell of the forewing densely pubescent in lower surface; marginal vein relatively short, 1.2 times as long as radial vein; body black with bronze tinge and in male, propodeum without costula, its median zone with uniform reticulation. P. bedeguaris is largely distributed in the Nearctic and Palaearctic regions. Caenacis inflexa (Ratzeburg, 1848) Material examined Azarbaijan-e-Sharghi Province, Marand, ex. leaf galls, on Rosa damascena, 17.viii.2003, (H. Lotfalizadeh), 8 & 1. Notes It was reared only on leaf galls of Rosa damascena and was not observed on fruit galls. BOUČEK & RASPLUS (1991) mentioned it as a species associated with cynipid galls on Rosa. Generally, it is parasitic on the larvae of the following cynipids: Diplolepis and Periclistus in galls of Diplolepis mayri on Rosa cinnamomea L. (GRAHAM, 1969). Fig. V Aximopsis collina: 1. Coxae in lateral view; 2. Male F1. Eurytoma rosae: 3. Male F1; 5. Coxae in lateral view. Eurytoma caninae: 4. Coxae in lateral view. Pteromalus bedeguaris: 6. Female profile in lateral view. Caenacis inflexa: 7. Female profile in lateral view.

10 82 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX The genus Caenacis can be distinguished morphologically by setose basal cell of the fore wing in distal half and strong costula on median area of the propodeum. This genus contains two species in the Palaearctic region. C. inflexa can be separated from C. lauta (Walker, 1835) by its long and sublanceolate shaped gaster (as long as head plus mesosoma) (fig. V, 7). Torymidae Three species belong to two genera Glyphomerus and Torymus (2 species) were identified. In addition, nine other species of Torymus were reported from Diplolepis galls in the Palaearctic region (Table 1). ZEROVA & SEREGINA (1992) also recorded Pseudotorymus rosarum on D. fructuum but we were unable to find it. However ASKEW et al. (2006) described a new species, Pseudotorymus regalis Askew, 2006 on D. mayri. In our key it can run to couplet 4 but with having hyaline forewing, one antennal anellus, 7-segmented funicule, distinct occipital carina can be distinguished from other species in the key. One specimen of an unknown species of Glyphomerus was collected in Peyam. We need further material to validate that this species is new for science. Glyphomerus stigma (Fabricius, 1793) ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 20 & 14. Same data, 12.ix.2003, 13 & 8. Azarbaijan-e- Sharghi Province, Zonuz, ex D. fructuum on R. canina, vii.1996, (H. Lotfalizadeh), 15 & 14. Tehran, Evin, ex D. fructuum on R. canina, 6.vi.2002, (H. Lotfalizadeh), 32 & 18. Notes This is a common species in Iran (RAKHSHANI et al., 2003; LOTFALIZADEH & GHARALI, 2005). The species was abundantly found in Marand region. The genus Glyphomerus includes seven species (ZEROVA & SERYOGINA, 1999; Noyes, 2002). G. carinatus Nikol skaya, G. tibialis Förster (PLANTARD, 1996; ZEROVA & SERYOGINA, 1999) and G. montanus Zerova & Seryogina (ZEROVA & SERYOGINA, 1999) were reported from rose galls. The species was recorded as a larval ectoparasitoid of several species of Diplolepis. It is widely distributed in Holarctic (SCHRÖDER, 1967; SHORTHOUSE, 1973 and NOYES, 2002) and was considered as an introduced species into Nearctic region (GRISSELL, 1995). GRISSELL (1995) considers this genus a primitive Toryminae which has Pteromalid-like wing venation (fig. VI, 1), simple hind femur, hind tibia with 2 apical spurs, occipital carina present but further than foramen (fig. VI, 2) and a single antennal anellus (fig. VI, 1). Torymus bedeguaris (Geoffroy, 1785) ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 2 & 1. Tehran, Evin, ex D. fructuum on R. canina, 11.vii.2002, (H. Lotfalizadeh), 1 & 1. Notes This common parasitoid of gall-maker cynipids on Rosa belongs to bedeguaris species-group; it was previously reported from Tehran Province (RAKHSHANI et al., 2003). GRISSELL (1995) recognized five species groups (belong 317 known species) for this genus with two groups, bedeguaris and tubicola presented in the Palearctic region. Recently, GRAHAM & GIJSWIJT (1998) revised 154 species in 13 species groups from Europe. The majority of them are associated with cynipid and cecidomyiid gall-makers. T. bedeguaris as an Holarctic species which emerge from a variety of cynipid galls on Rosa; is recorded for the first time from D. frutuum on Rosa canina. It is also reported as an hyperparasitoid of Wachtliella rosarum (Dip.: Cecidomyidae), Orthopelma mediator (Herting, 1977) and Periclistus pirates (SHORTHOUSE, 1973). Our collected specimens have the gaster coppery-green posteriorly, the hind femora infuscate, stigmal vein and parastigma vein darker than the rest (such as European specimens, see GRAHAM & GIJSWIJT, 1998) without brownish cloud around stigma. Torymus auratus (Müller, 1764) Material examined Azarbaijan-e-Sharghi Province, Peyam, ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 3 & 1. Azarbaijan-e-Sharghi Province, Zonuz, ex D. fructuum on R. canina, vii.1996, (H. Lotfalizadeh), 1. Notes It is a common parasitoid of many species of cynipid galls on oaks such as Andricus, Biorhiza, Cynips (GRAHAM & GIJSWIJT, 1998). D. fructuum on Rosa canina is a new host for the species. To be sure of our identification it was compared with reared specimens on oak gall wasps. It is widely distributed in Europe and GRAHAM & GIJSWIJT (1998) placed it in the bedeguaris species-group. Females of T. auratus differ from those of T. bedeguaris in having a gaster blue-green, and the legs yellow as indicated in the key to species. Ichneumonidae Orthopelma mediator (Thunberg, 1822) ex D. fructuum on R. canina, 5.v.2002, (H. Lotfalizadeh), 2. Same data, 12.ix.2003, 4 & 5. Same data, 22.iv.2005, 8 & 5. Notes Parasitoid of Diplolepis species. It is koinobiont endoparasit of eggs or young larvae of some Diplolepis species such as D. (PLANTARD, 1996). It is widely distributed in Europe (SCHRÖDER, 1967) (Table 3). Another species; Orthopelma brevicorne Morley has shorter antenna, 14-segmented antennal funicle (18-segmented in O. mediator) and parallel baso-medial carinae on the propodeum (as fig. II, 4 in O. mediator) is also reported from Diplolepis gall and can be confused with O. mediator. KEY TO THE ROSE-GALL ASSOCIATED WASPS IN THE STUDIED AREAS OF IRAN 1- Fore wing with a closed cell. Antenna filiform with more than 15 segments (figs. II, 1, 3, 5) Fore wing without closed cell (figs. III, 1 & 4; IV, 1, 3, 6, 7; V, 6, 7; VI, 1, 3). Antenna elbowed between the scape and pedicel with less than 15 segments (figs. III, 1, 4, 7; IV, 3; V, 6, 7; VI, 1, 3) Fore wing with open basal and sub-basal cells. Antenna with less than 18 segments. Gaster laterally compressed, on short petiole. Female with short ovipositor (fig. II, 1) Cynipidae Diplolepis fructuum Fore wing with close basal and sub-basal cells. Antenna 18- segmented. The first gastral tergite tapering into petiole at base, with long exerted ovipositor (fig. II, 3) Ichneumonidae (Orthopelma mediator)

11 Anno 2006 ROSE GALL WASPS AND THEIR ASSOCIATED FAUNA (HYMENOPTERA) IN IRAN Ovipositor longer than gaster. Hind coxa enlarged (figs. VI, 1 & 3) Torymidae Ovipositor shorter than gaster. Hind coxa not enlarged Fore wing distinctly infuscate. Anterior margin of metapleuron straight (fig. VI, 1). Body black Glyphomerus stigma Fore wing hyaline or slightly infuscate. Anterior margin of metapleuron S-shape (fig. VI, 3). Body bluish black with metallic tinge Legs brown. Gaster coppery or fiery Torymus bedeguaris Legs yellow. Gaster blue-green T. auratus 6- Mesopleuron convex and long, not impressed (fig. III, 6). Inner apical spur on hind tibia very long. Basitarsus of mid legs stout and with 1-2 row of fine pegs ventrally (fig. III, 5). Ovipositor visible (fig. III, 4) Eupelmidae Mesopleuron impressed, with femoral scrobe. Basitarsus of mid legs usual, without any pegs ventrally. Ovipositor very slightly exerted First and hind femora blackish-brown with distal pale band. Postmarginal vein not longer than stigmal vein. Scape blackish Eupelmus urozonus Femora and tibiae entirely pale. Postmarginal vein slightly longer than stigmal vein. Scape brownish Eupelmus fulvipes 8-Antennal funicle at most 4-segmented. Tarsi 4-segmented (fig. III, 1) Eulophidae Antennal funicle with more than 4 segments. Tarsi 5-segmented (fig. IV, 3) Funicular segments longer than wide. Gaster longer than mesosoma plus head. Last gastral tergite distinctly longer than its basal breath. Ovipositor distinctly exerted (fig. III, 3) Aprostocetus eurytomae Funicular segments subequal in length. Gaster shorter than mesosoma plus head and ovate (fig. III, 1), last gastral tergite slightly shorter than its basal breath. Ovipositor sheath very slightly exerted (fig. III, 2) A. aurantiacus 10- Body black. Head and mesosoma coarsely sculptured. Pronotum shoulder-like and long. Funicle 5-segmented in females (fig. IV, 3) Eurytomidae Body with metallic reflections (blue, bronze, green), with fine sculpture. Pronotum short and transverse. Funicle with more than 5 segments in females (figs. V, 6 & 7) Pteromalidae Marginal vein of forewing thickened. Wing membrane with infumated patch below it (fig. IV, 1) Sycophila biguttata Marginal vein of forewing normal and wing membrane hyaline below it Hind tibia with 2-3 long bristle-like hairs on its dorsal side (fig. IV, 2) Hind tibia without long bristle-like hairs on its dorsal side Notauli deep and groove-like. Scape distinctly swollen distally Notauli relatively superficial, step-like. Scape slightly swollen distally «Eurytoma» sp Piliferous punctures of scutellum relatively large in frontal margin of scutellum with 3 or less than 3 punctures «Eurytoma» sp.2 Piliferous punctures of scutellum normal on frontal margin of scutellum with more than 4 punctures «Eurytoma» sp Mesopleuron with ventral shelf (fig. IV, 4), anteriorly delimited by the epicnemial carina. Marginal vein not or hardly longer than the stigmal vein (fig. IV, 6) Aximopsis collina Mesopleuron without ventral shelf but with a sharp precoxal Fig. VI Glyphomerus stigma: 1. Female profile in lateral view; 2. Head and mesosoma in dorsal view. Torymus bedeguaris: 3. Fema le profile in lateral view.

12 84 H. LOTFALIZADEH - J.-Y. RASPLUS - G. DELVARE REDIA, Vol. LXXXIX tooth visible in lateral view (fig. IV, 5). Marginal vein longer than stigmal vein (fig. IV, 7) Clypeus slightly bilobed ventrally. Lower face mostly punctured. Mid coxae with evident lateral lamina (fig. V, 5). Medial propodeal furrow delimited laterally by distinct ridge E. rosae Clypeus slightly emarginated ventrally. Lower face with radiating ridges. Mid coxae without lateral lamina (fig. V, 4). Medial propodeal furrow without lateral ridge E. caninae 17- Basal cell of forewing dorsally hairy. Mesonotum and scutellum convex dorsally (fig. V, 7). Propodeum with some trace of costula. Flagellum and all of tibiae testaceous Caenacis inflexa Basal cell of forewing with sparse setae. Mesonotum and scutellum almost flat, laying in same plane (fig. V, 6). Propodeum without costula and reticulate medially. Flagellum dark-brown, tibiae dark-brown with testaceous distal band Pteromalus bedeguaris RIASSUNTO I CINIPIDI DELLA ROSA E LA FAUNA AD ESSI ASSOCIATA (HYMENOPTERA) IN IRAN I cinipidi della rosa (Diplolepis spp.) e la fauna ad essi associata è stata studiata nelle regioni settentrionali dell Iran per un periodo di oltre quattro anni. Durante questo periodo sono state raccolte e identificate 17 specie di Hymenoptera parassiti; di cui 11 specie risultano segnalate per la prima volta in Iran. Sedici specie appartengono alla superfamiglia Chalcidoidea, una sola specie agli Ichneumonoidea. Eurytoma collina Zerova, 1977 viene trasferita nel gen. Aximopsis (n. comb.). Viene anche presentata una breve rassegna dei parassitoidi associati con i cinipidi della rosa e questo complesso di specie viene comparato con i reperti di altre nazioni. Viene inoltre illustrata una rassegna dei parassitoidi associati alle specie del gen. Diplolepis su Rosa sp. della Regione Paleartica occidentale. 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