Chalcidoidea (Hymenoptera) obtained from common reed, Phragmites australis (Cav.) Trin. ex Steud. (Poaceae) in Iran with new records and descriptions of two new species

Fourteen species of Chalcidoidea (Encyrtidae, Eulophidae, Eupelmidae, Eurytomidae, Pteromalidae and Torymidae) were obtained from the common reed, Phragmites australis (Cav.) Trin. ex Steud. (Poaceae) in the Urmia region, in the northwest of Iran. Among these species, two new species of Pteromalidae are described hereafter: Norbanus persicus Lotfalizadeh & Rasplus sp. nov. and Stenomalina delvarei Lotfalizadeh & Rasplus sp. nov. Anagyrus near alienus Japoshvili, 2002, Asitus sp., Cheiloneurus paralia (Walker, 1837), Echthroplexiella obscura (Hoffer, 1952), Neococcidencyrtus poutiersi (Mercet, 1922) (all Encyrtidae), Aprostocetus orithyia (Walker, 1839) (Eulophidae), Eupelmus phragmitis Erdös, 1955 (Eupelmidae), Aximopsis deserticola (Zerova, 2004) comb. nov., Tetramesa phragmitis (Erdös, 1952) and Tetramesa sp. (all Eurytomidae), Homoporus febriculosus (Girault, 1917) (Pteromalidae) and Torymus arundinis (Walker, 1833) (Torymidae) were also obtained from our laboratory rearing. Nine of these species are recorded for the first time from Iran.


Introduction
The genus Phragmites Adans. (Poales, Poaceae) comprises the most common species of grasses (Poonawala et al. 1999). These monocot species are perennial, rhizomatous, stoloniferous and relatively tall (2.0-6.0 m). Among them, the common reed, Phragmites australis (Cav.) Trin. ex Steud., known as "Nei" in Persian, is a clonal and sub-cosmopolitan species (Clevering & Lissner 1999) and extremely abundant in the temperate regions (Haslam 1972). It is an invasive plant in some parts of its distribution, and there is a considerable body of scientifi c knowledge on its biology and ecology (Mal & Narine 2004;Kiviat 2013;Srivastava et al. 2013). Over the world, P. australis is known to host a huge diversity of insect species and at least 140 herbivorous species are associated with the common reed in Europe (Schwarzländer & Häfl iger 1999;Tscharntke, 1999;Tewksbury et al. 2002), causing signifi cant damage. Among these insect species, more than 70%, attack the leaves and the stems (Tewksbury et al. 2002). Schwarzländer & Häfl iger (1999) revealed that 50% of these phytophagous species are specialists, associated only with the genus Phragmites. Tewksbury et al. (2002) considered that 40% of the species associated with Phragmites are monophagous, and that Diptera Linnaeus, 1758 (with 55 species) and Lepidoptera Linnaeus, 1758 (with 45 species) are the two most represented insect orders. Several phytophagous species associated with Phragmites are rhizome-feeders, e.g., lepidopterous and some others stem-borers, e.g., moths and chloropid fl ies (Barczak et al. 2013). These phytophagous insects have been investigated for their effi ciency in controlling of P. australis in North America (Tewksbury et al., 2002) and at least two species of European noctuid moths viz., Archanara geminipuncta Haworth, 1809 andA. neurica (Hübner, 1808) are being tested as potential biological control agents in North America.
However, little attention has been given to the numerous parasitic wasps that parasitize the phytophagous insects associated with Phragmites spp. Among them, Chalcidoidea Latreille, 1817 (Hymenoptera) is the most represented superfamily and about 152 species belonging to 10 families of chalcid wasps have been cited worldwide. About 39% of associated Chalcidoidea with Phragmites spp. (61 species from 9 families) have been reported with phytophagous insects on Phragmites australis (Table 1) (Noyes 2020). While most of the chalcid species are parasitoids, Tetramesa spp. (Hym.: Eurytomidae) are phytophagous.
The aim of this study was to investigate the parasitic community associated with some phytophagous insects developing in the common reed in Iran. Our study is a fi rst step towards a more comprehensive survey and we here describe the diagnostic characters of these wasps for future bio-ecological studies.

Material and methods
Preliminary probes to fi nd overwintered and attacked stems of common reed by splitting them had shown that stems with a maximum height of 50 to 120 cm were more infected than higher and fl owered stems. Upon awareness of this, we started to collect the likely attacked samples of reed stems at several times during March-April of 2016. Samples were picked out from about 50 cm from the top of the stems whose maximum height was between 40 and 140 cm. About 500 samples of reed stems were collected in nine dry/moist and dense /rare reed stands from four different sites on the edges of farmlands and abandoned areas in the Urmia region: Orümïyeh, Azarbaijan-e Gharbi (= West-Azarbaijan) Province, Iran. The sites and their geographical coordinates (Anonymous 2006) are given below: The reared chalcidoids were identifi ed using the keys of Ferrière (1955), Claridge (1958), Zerova (1976Zerova ( , 2010, Graham (1987), Noyes (1987), Bouček & Rasplus (1991), Graham & Gijswijt (1998), Trjapitzin (2006, Zerova & Seryogina (2006), Rizzo & Mitroiu (2010), Mitroiu (2015) and Gibson & Fusu (2016).
The type material and all studied specimens are deposited in the HMIM (Hayk Mirzayans Insect Museum, Tehran, Iran) and in CBGP insect collection (Centre de Biologie pour la Gestion des Populations, Montferrier-sur-Lez, France). Identifi ed families, genera and species were listed alphabetically.

Remarks
Our specimens possess all the diagnostic characters of A. alienus, but the females are slightly larger (2.2 mm) than the type specimens of A. alienus (1.7 mm). Furthermore, the scape ( Fig. 1B) is also slightly wider than in A. alienus (about 2.5 × vs 3.3 × as long as broad in A. alienus), consequently our specimens could represent an undescribed species. Anagyrus alienus was previously known from Turkey and our sampling locality is close to the type locality. The biology of A. alienus is unknown (Japoshvili 2012). Our sampling reveals an association of A. near alienus with P. australis, on which it is associated with a species of Pseudococcidae (Hemiptera) that appears to be a pest of P. australis.

Remarks
Asitus phragmitis (Ferrière, 1955) is a parasitoid of Pseudococcidae on Phragmites australis in the Caucasus, several European countries, USA and Pakistan (Ferrière 1955;Guerrieri 1989;Noyes 2020). Our specimen is closely related to A. phragmitis and shares several characters with that species: body   (Ferrière, 1955).  dorsoventrally fl attened; head prognathous, head and mesosoma fi nely reticulate; antennae inserted just above clypeus and widely separated from each other; pronotum divided into two subtriangular parts; notauli absent; scutellum wider than long, about 1.9 × as wide as long, anteriorly reaching the base of the tegula. However, it differs from A. phragmitis in several characters (Table 2) and in our opinion very probably represents a new species. Because we only sampled a single male, we will not describe this species and await further samples.

Remarks
This species is distributed in the north and east of Europe (Askew 1970;Kalina 1989;Trjapitzin 1989) and represents a new record from Iran. The biology of E. obscura is still unknown, but the species could be associated with a pseudococcid species on P. australis.

Remarks
This species is only known from Turkmenistan and is a parasitoid of Diaspididae Targioni-Tozzetti, 1868 (Hemiptera Linnaeus, 1758) (Noyes 1987(Noyes , 2020. This is the fi rst record for Iran. The species is about 2 mm long; brachypterous ( Fig. 5A-B), fore wing mostly infuscate with interrupted hyaline fascia, venation extending over at least two-thirds of wing, linea calva interrupted by 2-3 setae; fronto-vertex in dorsal view narrower than the eye width (Fig. 5B); funicle in female 6-segmented, F6 about 2 × as broad as the fi rst segment and much broader than the pedicel (Fig. 5C).

Remarks
Aprostocetus orithyia is only known from Europe, develops on fl y larvae (Cecidomyiidae and Chloropidae) and this sampling represents a new record for Iran. Aprostocetus orithyia belongs to the lycidas species group (Graham 1987). On P. australis, the species could be a parasitoid of the aforementioned dipterous families.
Main morphological characters: body generally metallic with yellowish tibiae and tarsi ( Fig. 6A), antenna with scape as long as the eye, reaching above the level of vertex; funicle very long and slender, 3-segmented, F1-F2 3.05 ×, F3 about 2.6 × as long as broad (Fig. 6B); clava with a relatively shorter and less conspicuous, straight terminal spine. Mid lobe of mesoscutum strongly reticulate ( Fig. 6F), areoles of reticulation about 3-4 × as long as broad, with a median line, and a single row of adnotaular setae on each side. Fore wing apically ciliate, submarginal vein with 2 dorsal setae, speculum absent. Spur of mid tibia longer than half the length of the basitarsus and distinctly longer than the width of the tibia. Metasoma as long as head plus thorax (Fig. 6A).

Remarks
Eupelmus phragmitis is distributed in the Czech Republic, Greece, Hungary, Israel, Romania, Ukraine and South Korea, and is a parasitoid of Tetramesa phragmitis (Hym.: Eurytomidae) (Gibson & Fusu 2016). The species may be associated with the same host on P. australis in Iran.
This species belongs to the stramineipes species group (Gibson & Fusu 2016). All the features of the sampled specimen well match those reported by Gibson & Fusu (2016), in the couplet 18. It shares the following combination of characters: scrobal depression obviously more deeply reticulate than frontovertex; antennal scape entirely dark, clava lighter than funicle, anellus slightly longer than wide, similarly dark as rest of funicle; fore wing hyaline, infuscate below marginal and stigma veins, dorsally with basal cell and disc uniformly setose except for linea calva, with complete marginal fringe, marginal vein much longer relative to stigma vein; legs sometimes with all femora similarly yellow; ovipositor sheath pale, apparent length of ovipositor sheath distinctly shorter than metatibia. However, it has the following variations: body metallic green ( Fig. 7A-B) with obviously golden refl ections and reddish- violet refl ections on the scrobal depression, tegula brownish-yellow, legs more extensively pale, slightly darker femur and tibiae medially; F1 less transverse, clava slightly lighter than the rest of antenna (Fig. 7C).

Remarks
The species has been reported from fruits of Cuscuta approximata Bab. (Cuscutaceae) in Tajikistan and Turkmenistan (Zerova 2010).
This species has characters of the nodularis species group (Lotfalizadeh et al. 2007), and with sharing conspicuous mesopleural shelf, carinate fore coxae and distinctly petiolate gaster, it is consequently transferred from Eurytoma Illiger, 1807 to the genus Aximopsis. Aximopsis deserticola can be separated from closely related species by the following set of characters: head round and slightly wider than long in frontal view (Fig. 8B); inner orbital margin coarsely punctate, and appearing to be slightly carinate; all funicular segments in female distinctly longer than wide (Fig. 8E), F1 about 2.5 × as long as its width; fore coxa distinctly carinate in frontal view; mesopleuron with an obvious ventral shelf, carinate anteriorly and with an oblong comb anteromedially (Fig. 8D); marginal vein as long as postmarginal vein, slightly longer than stigmal vein, postmarginal vein about 1.5 × as long as stigmal vein (Fig. 8C); metasoma of female rounded, as long as mesosoma in lateral view (Fig. 8A), with long petiole, slightly longer than wide.
This species has recently been redescribed (Zerova & Fursov 2016)  with yellow spots reduced to head, below eyes and lower face (Fig. 9A, E) vs yellow spots on head and thorax, also much lighter specimens occur in Israel and Tajikistan (Zerova & Fursov 2016). Fore wing (Fig. 9C) mainly infuscate with two distinct dark spots, the fi rst one under marginal and stigmal veins and the second as a V-shaped dark spot below submarginal vein vs unclear yellow spot under marginal vein (Zerova & Fursov 2016); and distinctly dark-brown veins vs yellowish veins (Zerova & Fursov 2016).

Remarks
Only T. phragmitis has previously been reported from Phragmites spp. (Noyes 2020). Based on the key of Claridge (1961), our specimens are closely related to Tetramesa cornuta (Walker, 1832) in the couplet 17, sharing with this species the following characters: funicular segments short with F5 quadrate; pronotum transverse (Fig. 10D), about 2 × as wide as long; mid tibial spur relatively long, longer than half length of basitarsus; longer GT3 non-emarginate posteriorly. However, the female appears to be larger than is reported for T. cornuta; marginal vein at most as long as stigmal vein (vs marginal vein twice as long as stigmal vein in T. cornuta); metasoma longer than the combined length of head plus mesosoma (75:65) (vs metasoma shorter than combined length of head and mesosoma in T. cornuta).
In the male, the funicular segments are slightly longer than in the female (Fig. 10C) but a more distinct sexual dimorphism was observed in T. cornuta (Claridge 1961: fi gs 97-98). This species clearly is different from T. cornuta and may be new. However, further specimens are required and we also need to examine several type specimens belonging to the genus Tetramesa to ascertain its novelty.

Remarks
Homoporus febriculosus is a Palaearctic species that is distributed from UK to Turkey and also reported from Canada (Noyes 2020). It is known as a parasitoid of some Diptera (Agromyzidae, Cecidomyiidae, Chloropidae) and Hymenoptera (Braconidae Latreille, 1829, Cephidae Newman, 1834 and Eurytomidae) and in our rearing, it seems to be parasitoid of Tetramesa spp. (Eurytomidae) and Lipara spp. (Chloropidae) associated with P. australis.
All the characters of the sampled specimens well match those reported by Gahan (1933) with the following variations: much larger, body length of females vary from 3.3 to 3.8 mm and males from 2.5 to 3.17 mm vs female 2-2.8 mm and males 1.2-2.3 mm (Gahan 1933); head and mesosoma dark, with slight metallic greenish-blue to violet tinge versus dark metallic green (Gahan 1933

Diagnosis
Relatively large species (3.45-4.17 mm); metallic green mesosoma and brown metasoma; in female all funicular segments long longer than broad, F1 about 3.7 × as long as broad; in male funicular segments fi liform, long and not pedicellate; clypeus dorsally strigose; hind margin of fi rst tergite straight or slightly convex in posterior part; fore wing of male and female with basal cell and basal vein entirely bare especially in basal half, postmarginal vein shorter than marginal vein.

Etymology
This species is named after the ancient name of Iran (Persia). COLOR. Head and mesosoma black, with slight metallic greenish refl ections, metasoma brown without metallic refl ections. Eyes brownish. Ocelli honey-yellow. Pilosity on the body long and whitish. Mandibles brown, teeth dark brown. Antenna (Fig. 13C) brown with scape, light brown to yellow distally, clava yellow. Coxae brown, femora brown medially and yellow apically and basally, all tibiae and tarsi pale yellow, claws and arolia darker. Wings hyaline, tegula and wing venation yellowish-brown (Fig. 14D), wing setae dark.

Variation
Body length of females varies from 2.67-5.40 mm and males from 3.45-4.17 mm. Antennae of female in smaller specimens entirely yellow. Metasoma and femura of female dark-brown to dark in some specimens. Metasoma of males darker than females. Wings slightly fuscate, especially in larger specimens but entirely hyaline in smaller specimens.

Biological association
Host unknown. This species was reared from Phragmites australis in northwest Iran. Within the reared phytophagous insects, Chilo phragmitella (Hübner, 1810) (Lepidoptera: Crambidae) is its most likely host.

Distribution
Only known from Iran.

Remarks
The species closely resembles N. tenuicornis Bouček, 1970 known from Europe, Africa and China. It mainly differs in body size and coloration, and some antennal characters. Detailed diagnostic features of both species are provided in Table 3.
The male of this species is similar to that of the genus Gugolzia Delucchi & Steffan, 1956 in having the antennae inserted far above the center of the face, but the distinct antennal spicula of N. persicus Lotfalizadeh & Rasplus sp. nov. (less visible in Fig. 14C, due to whorls of long and dense setae) runs it to the group of pteromalids with spiculated antennae that males in the genus Gugolzia miss. In addition, the

Diagnosis
Clypeus medially pointed and with lateral teeth, dorsally fi nely strigose; malar space slightly more than half the length of an eye; pedicel + fl agellum 0.9 × as long as head width, elongate funicular segments (distinctly longer than wide); temple converging slightly behind the eye dorsally, slightly more than ⅓ as long as eyes; propodeum, with an inverted Y-shaped median carina; costal cell ventrally with three rows of short setae near dorsal margin; basal third of wing bare, postmarginal vein longer than marginal and stigma veins; metasoma lanceolate, short, 1.7 × as long as broad, relatively shorter metasoma (shorter than head + mesosoma).

Variation
Body length of females based on available specimens varies from 3.85 to 4.07 mm.

Biological association
Host unknown. This species was reared from Phragmites australis in northwest Iran. Species of Chloropidae are its most likely host.

Distribution
Only known from Iran.

Remarks
The female is closely related to females of Stenomalina rossiliensis Graham, 1986 andS. liparae (Giraud, 1863) also reared from Phragmites australis, and may be separated by the following key:  Graham, 1986 Stenomalina delvarei Lotfalizadeh & Rasplus sp. nov. shares the following characters with S. rossiliensis: elongate funicular segments (more than 1.3 × as long as wide) and the sculpture of the propodeum, with an inverted Y-shaped median carina. Considering some morphological characters mentioned by Graham & Claridge (1965), this species is similar to Stenomalina liparae and shares the following characters: malar space slightly more than ½ as long as eye; elongate funicular segments; temple converging slightly behind the eye dorsally, slightly more than ⅓ as long as eyes; lanceolate metasoma, relatively shorter metasoma (shorter than head + mesosoma). Family Torymidae Walker, 1833 Subfamily Toryminae Walker, 1833 Genus Torymus Dalman, 1820

Remarks
Torymus arundinis is widely distributed in Europe, but has not yet been reported from the Middle East (Noyes 2020), our specimens represent a new record for Iran. The species may be a parasitoid of Cecidomyiidae (Diptera) on P. australis.

Discussion
This is the fi rst effort to study Chalcidoidea associated with P. australis in Iran. Furthermore, the family Encyrtidae with the maximum presence of species (4 spp.) revealed that in this area their hosts (mostly Hemiptera) could be the main pests of P. australis. Myartseva (1982) reported 13 species of Encyrtidae in Turkmenistan. Based on the present study, only 21% of obtained chalcidoids (two species of Tetramesa) are the pest of P. australis and the rest are parasitoids of other insects Therefore, supplementary investigations are highly advised to reveal the biological association of these parasitoids with supposed insect pests of the families Agromyzidae, Chloropidae, Crambidae, Cecidomyiidae, Mordellidae and Pseudococcidae.
Within the identifi ed species, Aprostocetus orithyia and Norbanus persicus Lotfalizadeh & Rasplus sp. nov. were the most abundant, that may be parasitoids of Cecidomyiidae and Crambidae, respectively. Finally, the species which have been introduced in this study were collected and identifi ed from a limited area in northwestern Iran. Iran is very diverse in terms of climatic conditions and topography, and the reed plant is spread in many areas of country. Given this diversity, there is no doubt that herbivorous insects associated with reeds and their parasitoids have a considerable diversity throughout Iran, and further studies in different parts of Iran will lead to further identifi cations of new species and new records as well.