Turkish Journal of Zoology Turk J Zool (2017) 41: 345-353 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Short Communication doi:10.3906/zoo-1605-35

Discovery of the genus Mirodryinus Ponomarenko, 1972 (Hymenoptera, Chrysidoidea, Dryinidae) associated with salt cedar trees in the eastern part of Iran

1 1, 2 1 Hossein Ali DERAFSHAN , Ehsan RAKHSHANI *, Massimo OLMI , Mehri VAFAEI 1 Department of Plant Protection, College of Agriculture, University of Zabol, Zabol, Iran 2 Tropical Entomology Research Center, Viterbo, Italy

Received: 17.05.2016 Accepted/Published Online: 28.07.2016 Final Version: 04.04.2017

Abstract: In 2015 and 2016 a survey was carried out on the parasitoids of (, ) feeding on salt cedar trees (Tamarix spp.) growing around Hamoon Lake in the Sistan region (Iran). Among the collected material, a series of dryinid specimens belonging to Mirodryinus atlanticus Olmi, 1984 (Hymenoptera, Dryinidae, Bocchinae) was captured on branches of Tamarix aphylla (L.) Karst. and Tamarix stricta Boiss., infested by versicolor (Distant) (Hemiptera, Cicadellidae). The subfamily Bocchinae and the genus Mirodryinus Ponomarenko, 1972 are new records for Iran. Diagnostic characters and notes on the morphological variability of the newly collected specimens are presented and discussed.

Key words: Bocchinae, , Opsius, Tamarix, Mirodryinus atlanticus, wetland, Hamoon Lake

Dryinidae (Hymenoptera, Chrysidoidea) is a Various species of Tamarix grow in different parts moderately large family with worldwide distribution and of Iran. Among them, some species are associated with 15 extant and extinct subfamilies (Olmi and Virla, 2014; wetlands and salty soils. The studied area is that around Olmi and Xu, 2015). The subfamily Bocchinae Richards, Hamoon Lake (Sistan and Baluchestan Province), 1939 includes 104 species belonging to three genera (Olmi including habitats dominated by some species of salt cedar and Xu, 2015): Bocchus Ashmead, 1893; Mirodryinus trees (Tamarix spp.). Tamarix species have extraordinary Ponomarenko, 1972; and Mystrophorus Förster, 1856. biological features and adaptive capabilities to wetlands Mirodryinus is a very small Palearctic genus including eight and salty soils (Fornasari, 2004). from different known species: M. atlanticus Olmi, 1984 (known from the orders have been known in association with Tamarix Canary Islands, Egypt, Morocco, Tunisia, Turkmenistan, species as a primary trophic level (Fornasari, 1998; and the United Arab Emirates); M. gobiensis Ponomarenko, Wiesenborn, 2005). Among the associated , a 1972 (known from Kazakhstan and Mongolia); M. kerzhneri moderately well-defined assemblage of leafhoppers was Ponomarenko & Olmi, 2006 (known from Kazakhstan); recorded feeding on Tamarix species (Virla et al., 2010; M. olmii (Móczár, 1983) (known from Mongolia); M. Sher and Quigley, 2013; Mozaffarian and Wilson, 2016). ponomarenkoae Olmi, 1984 (known from Mongolia and Wasps of the family Dryinidae (Hymenoptera, Uzbekistan); M. tussaci Olmi, 1990 (known from Morocco); Chrysidoidea) are known as natural enemies of M. ungulatus Ponomarenko, 1972 (known from Algeria); leafhoppers, planthoppers, and treehoppers (Hemiptera, and M. xerophilus (Benoit, 1951) (known from Egypt and ) (Guglielmino et al., 2013). While many Libya). Keys of the Bocchinae genera are available from species of leafhoppers are recorded from Iran (Mozaffarian Olmi (1999). Keys of Mirodryinus species are present in the and Wilson, 2011, 2016), very few species of dryinids are works of Olmi (1984, 1999) and Olmi and Xu (2015). documented. According to the most recent revisions of the Most dryinids are generalists attacking a wide variety Eastern (Olmi and Xu, 2015) and Western (Olmi, 1999) of Hemiptera Auchenorrhyncha (Guglielmino and Olmi, Palearctic regions, only six dryinid species are recorded 1997). On the contrary, Mirodryinus includes species from Iran. Recent surveys revealed additional dryinids apparently developing exclusively on Opsius Fieber from Iran including new taxa (Derafshan et al., 2016). In the (Cicadellidae, , ) (Guglielmino and most recent paper (Derafshan et al., 2016), a new species of Olmi, 1997, 2007; Guglielmino et al., 2013, 2015). the family Dryinidae (Dryinus tamaricicola Rakhshani & * Correspondence: [email protected] 345 DERAFSHAN et al. / Turk J Zool

Olmi, 2016) was found in association with salt cedar trees triangular cards. Slides of the forewing and foreleg were of the Hamoon wetland. In this paper we record additional prepared to study the morphological details. The external species of dryinids belonging to the subfamily Bocchinae morphology of specimens was studied using Nikon in association with common leafhoppers living in Tamarix SMZ645 stereomicroscope. Illustrations were taken using forests around Hamoon Lake (Sistan region, Iran). a Hund Wiloskop equipped with a BMZ-04-DZ digital The scope of this paper is a contribution to the imaging system (Behin-Pajouhesh Co., Iran). A series of knowledge of Iranian Dryinidae, not only from a 4–8 captured images was merged into a single in-focus biogeographic and systematic point of view but also to image using the image-stacking software Zerene Stacker establish the first basis for biological control projects by version 1.04. The morphological terminology follows that dryinids in Iran against leafhoppers pests of cultivated of Olmi and Xu (2015). plants. Parasitized specimens of Opsius were collected by sweep Samplings were performed in 2015 on salt cedar trees net on Tamarix in the above sites around the Hamoon growing around the Hamoon wetlands in the Sistan region wetlands. They were reared to check that the parasitoid (Zabol, Sistan and Baluchestan Province, Iran) (Figure 1). was Mirodryinus atlanticus. Rearing tubes were provided Specimens of Dryinidae were collected by a sweep net with Tamarix leaves for feeding Opsius specimens. They on Tamarix aphylla (L.) Karst. and Tamarix stricta Boiss. were kept in laboratory conditions. The specimens were then captured using an aspirator Specimens were deposited in the collection of the and dropped into 75% ethanol for subsequent studies. Department of Plant Protection, University of Tuscia, Afterwards, the specimens were prepared according to Viterbo, Italy (Massimo Olmi’s collection - MOLC) AXA methods (van Achterberg, 2009) and mounted on and partly in the collection of the Department of Plant

Figure 1. The sampling locations around Hamoon Lake (Sistan), represented by natural and cultivated Tamarix species.

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Protection, College of Agriculture, University of Zabol, - Segment 5 of protarsus only with bristles, without Iran (DPPZ). lamellae (figure 447 in Olmi, 1984) ...... M. olmii (Móczár) Subfamily Bocchinae Richards, 1939 3 Forewing with stigmal vein curved, with distinct Key to the genera of Bocchinae (females and males) proximal and distal parts ...... 4 (from Olmi, 1999) - Forewing with stigmal vein straight, only with distinct FEMALES proximal part (figures 438, 439 in Olmi, 1984) ...... 7 1 Segment 5 of protarsus with inner membranous band 4 Forewing hyaline, not crossed by dark transverse (figure 410 in Olmi, 1984); occasionally without inner bands, with distal part of stigmal vein longer than proximal membranous band, then with one only preapical lamella part ...... M. tussaci Olmi (figure 419 in Olmi, 1984) ...... Bocchus Ashmead - Forewing crossed by dark transverse band, with distal - Segment 5 of protarsus without inner membranous part of stigmal vein as long as or shorter than proximal band (figures 442, 451, 456 in Olmi, 1984), with rows of part ...... 5 bristles (figure 442 in Olmi, 1984) or peg-like hairs (figure 5 Mesosoma completely black ...... 456 in Olmi, 1984), with distal apex provided with group ...... M. gobiensis Ponomarenko of lamellae or bristles (figures 451, 456 in Olmi, 1984), - Mesosoma completely or partly reddish ...... 6 never with only one preapical lamella . . . 2 6 Mesosoma completely reddish; notauli reaching 2 Fully winged (figures 438, 449 in Olmi, 1984) ...... approximately 0.5 length of scutum ...... Mirodryinus Ponomarenko ...... M. kerzhneri Ponomarenko & Olmi - Apterous, or micropterous (figures 452, 453 in Olmi, - Mesosoma partly reddish and partly black; notauli 1984) ...... Mystrophorus Förster reaching approximately 0.2–0.3 length of scutum ...... MALES ...... M. atlanticus Olmi 1 Forewing reduced (figure 454 in Olmi, 1984) or 7 Mesosoma completely reddish ...... absent ...... Mystrophorus Förster ...... M. xerophilus (Benoit) - Forewing complete (figures 402, 440 in Olmi, 1984) - Mesosoma partly reddish and partly brown or black .. . . . 2 ...... 8 2 Genitalia with distivolsella articulated with distal 8 Scutum brown ...... M. ungulatus Ponomarenko margin of basivolsella (figure 444 in Olmi, 1984); - Scutum reddish ...... 9 propodeum with areolae very small, less wide than tegulae .. 9 Metapleuron reddish, occasionally partly darkened ...... Mirodryinus Ponomarenko ...... M. atlanticus Olmi - Genitalia with distivolsella articulated along - Metapleuron black ...... M. ponomarenkoae Olmi inner margin of basivolsella (figure 431 in Olmi, 1984); MALES propodeum with areolae very wide, at least as wide as 1 Stigmal vein of forewing with long proximal part tegulae . . . Bocchus Ashmead and very reduced distal part (figure 2 in Olmi, 1990); Genus Mirodryinus Ponomarenko, 1972 propodeum strongly reticulate rugose . . . M. tussaci Olmi Both males and females of the known species with - Stigmal vein of forewing with only proximal part, developed wings. Forewing with three closed cells; distal part absent (figures 440, 441 in Olmi, 1984; figure 3 pterostigma visible; mandibles with four teeth, one in Olmi, 1990) ...... 2 rudimentary tooth present between the two posterior 2 Propodeum completely and strongly reticulate rugose teeth; occipital carina complete and visible. Last protarsus ...... M. atlanticus Olmi segment without inner membranous band, bearing rows - Propodeum slightly and irregularly sculptured by of bristles or peg-like hairs, with distal apex provided with keels, not completely and strongly reticulate rugose ...... lamellae or bristles. Enlarged claw bare, without lamellae, ...... M. xerophilus (Benoit) bristles, hairs, or peg-like hairs. Remark: The species not present in both above keys Distribution: Palearctic. are known from only one sex. Species: Eight. Mirodryinus atlanticus Olmi, 1984 Key to the species of Mirodryinus Material examined: 4♀, IRAN, Sistan and Baluchestan FEMALES Province, Zabol, Hamoon wetlands (31°09′23.7″N, 1 Forewing with stigmal vein absent (figure 448 B in 61°23′57.9″E, 450 m), swept on Tamarix aphylla, Olmi, 1984) ...... 2 14.10.2015, leg. H.A. Derafshan (MOLC); 9♀ and 1♂, - Forewing with stigmal vein distinct (figures 438, 439, same data, 14.03.2016 (DPPZ); 6♀, same data, 13.05.2015 448 A in Olmi, 1984) ...... 3 (DPPZ); 1♀ and 1♂, same data, 15.05.2015 (DPPZ); 2♀, 2 Segment 5 of protarsus with lamellae and bristles same data, 21.10.2015 (DPPZ); 1♀, same data, 23.11.2015 (figure 446 in Olmi, 1984) ...... M. atlanticus Olmi (DPPZ); 10♀ and 1♂, same data, 13.03.2016 (DPPZ); 9♀

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Figure 2. Habitus of Mirodryinus atlanticus Olmi (female specimen): A) lateral view of head; B) face; C) dorsal view of head; D) mesosoma in lateral view; E) mesosoma in dorsal view; F) forewing; G) propodeum and petiole; H) protarsus and chela.

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Figure 3. Mirodryinus atlanticus Olmi: general habitus in lateral view: A) male; B) female. and 1♂, same data, 14.03.2016 (DPPZ); 3♀, same data, of pterostigma; marginal cell closed. Propodeum (Figure 05.04.2016 (DPPZ); 3♀, same data, 10.04.2016 (DPPZ); 2G) with reticulated fine sculpture. First protarsomere 14♀, same data, 19.04.2016 (DPPZ); 10♀, same data, (Figure 2H) as long as or slightly longer than all other 20.04.2016 (DPPZ); 1♀, same data, 27.04.2016 (DPPZ); segments together, with proximal hollow (=antennal 6♀, same data, 18.04.2016 (DPPZ); 2♀, IRAN, Sistan cleaner) immediately after basal projection. Enlarged claw and Baluchestan Province, Zabol, Hamoon wetlands without bristles and lamellae. Last protarsomere with 1 (31°12′04″N, 61°20′41″E, 477 m), swept on Tamarix stricta, row of about 18 lamellae and 1 row of 7 bristles; distal apex 03.04.2016 (DPPZ); 4♀, IRAN, Sistan and Baluchestan with approximately 4–10 lamellae. Tibial spurs: 1/1/1. Province, Zabol, Nimrooz (31°05′04″N, 61°26′04″E, 477 Metasoma glabrous, lanceolate (Figure 3A), as long as m), swept on weeds, 14.03.2016 (DPPZ); 4♀, same data, head and mesosoma together, with petiole well developed, swept on Tamarix aphylla, 14.05.2016 (DPPZ); 3♀, IRAN, widened towards the base and with deep central keel. Sistan and Baluchestan Province, Zabol, Hamoon wetlands Coloration: Head brown; mandible whitish with dark (31°09′03.5″N, 61°22′46.9″E, 450 m), swept on Tamarix teeth; lower margin of eyes close to anterior margin of face stricta, 05.04.2016 (DPPZ), 4♀, same data, 21.03.2015 whitish; antenna dark brown or black, except segments 1–2 (DPPZ), leg. H.A. Derafshan. yellowish brown; mesosoma reddish brown; metanotum Short description: Female (Figures 2A–2H) – Head partly black; legs reddish brown, except metafemur and transverse, finely punctate, with occipital carina complete metatibia dorsally dark brown; wings hyaline; forewing (Figures 2A, 2C); face (Figure 2B) hairy; frontal line with dark area extended from pterostigma to distal margin, absent; area between antennal toruli with dense hairs; gradually effaced; metasoma black. clypeus wide, convex, and covered with long hairs; eyes Body length: 2.55–2.65 mm. large (Figure 2B), projected from lateral sides; OOL/ Male (Figures 3B, 4A–4G): Similar to the female, but POL: 1.3; antenna 10-segmented, clavate, with scape with dark color; tibial spur 1/1/2. slightly curved outwardly and almost twice as long as Distribution: Egypt, Morocco, Spain, Tunisia, pedicel; flagellomere I slightly longer than II; remaining Turkmenistan, United Arab Emirates (Olmi and Xu, flagellomeres gradually shortening. Pronotum (Figures 2015), Iran (new record). 2D, 2E) short, with transverse central dorsal depression, Reared material: Parasitized nymphs of Opsius finely striated, sparsely hairy, with lateral posterior versicolor (Distant) (Cicadellidae, Deltocephalinae, tubercle reaching tegula. Scutum and scutellum smooth. Opsiini) (Figure 5) collected from the same host plant Notauli incomplete (Figure 2E), only visible in anterior (Tamarix aphylla) from which we captured the adult region of scutum. Forewing (Figure 2F) with pterostigma specimens of Mirodryinus atlanticus. Live specimens were subtriangular and stigmal vein straight and as long as height reared in laboratory conditions for possible emergence of

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Figure 4. Habitus of Mirodryinus atlanticus Olmi (male specimen): A) lateral view of head; B) face; C) dorsal view of head; D) mesosoma in lateral view; E) mesosoma in dorsal view; F) forewing; G) propodeum and mesosoma. the adult parasitoids. Few cysts attached to the nymphs Mirodryinus atlanticus is newly recorded here from hatched naturally and the larvae pupated inside the sandy Iran. It belongs to a genus and a subfamily (Bocchinae) soil provided on the bottom of the rearing boxes. No adults found for the first time in Iran. Two other subfamilies, emerged after several experiments during two subsequent Dryininae and Gonatopodinae, have already been recorded years, 2015 and 2016. from Iran (Olmi and Xu, 2015). According to Olmi and

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Figure 5. A, B) Nymphs of Opsius versicolor (Distant) probably parasitized by Mirodryinus atlanticus Olmi (in B. thylacium opened after emergence of a mature larva); C) mature larva of M. atlanticus.

Xu (2015), the following six species are recorded from known parasitoid of Opsius species feeding on Tamarix Iran: Dryinus gharaeii Olmi, 2005 (Dryininae); Gonatopus (Guglielmino et al., 2013; Olmi and Xu, 2015). A similar camelinus Kieffer, 1904;G. clavipes (Thunberg, 1827);G. host association was already recorded from Morocco distinguendus Kieffer, 1905;G. iranicus Olmi, 1984; and (Guglielmino and Olmi, 1997). A successful rearing Haplogonatopus apicalis Perkins, 1905 (Gonatopodinae). of Opsius versicolor parasitized nymphs is necessary to Recently, Derafshan et al. (2016) recorded two further confirm that M. atlanticus is the associated parasitoid. Dryinus species (Dryinus tamaricicola Rakhshani & Olmi, Dryinidae taxa have high potential as biological 2016 [in Derafshan et al., 2016] and Dryinus tarraconensis control agents. The predatory and parasitic efficiency of Marshall, 1868). The present contribution revealed the this family has been studied in many species (Olmi, 1994, presence of the Bocchinae as the third subfamily in Iran. 1999). As examples of the efficiency of Dryinidae, there According to the general distribution of Bocchinae and are the following data: for Gonatopus flavifemur (Esaki and Mirodryinus (Olmi and Xu, 2015), further species are Hashimoto, 1932) (Gonatopodinae), the female can kill 466 probably present in Iran. specimens of Nilaparvata lugens (Stål) (a famous rice pest The specimens of M. atlanticus studied in the present in Asia) during its lifetime (about 12 days): 418 parasitized, paper were collected from March to May and in October 48 preyed (Chua and Dyck, 1982). For Neodryinus and November. In summer, from June to September, and typhlocybae (Ashmead, 1893) (Gonatopodinae), the winter, from December to February, no specimens of M. female can kill 70 specimens of Metcalfa pruinosa (Say) (a atlanticus were found, probably because of the respectively famous Nearctic pest of cultivated shrubs introduced into high and low temperatures. Europe) during its lifetime (about 20 days): 30 parasitized, The collected specimens of M. atlanticus were always 40 preyed (Girolami and Conte, 1999). found among colonies of Opsius versicolor, which is Dryinids have been used in biological control the probable host, as this dryinid species is a well- programs in four instances (Olmi, 1999). In 1906 and

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1907 Pseudogonatopus hospes Perkins, 1912 (now a junior biological data were reported by Olmi (1994, 1999), Olmi synonym of Gonatopus nigricans (Perkins, 1905)) and and Virla (2014), Olmi and Xu (2015), and Xu et al. (2013). Haplogonatopus vitiensis Perkins, 1906 were introduced Records of parasitization of leafhoppers by Bocchinae into Hawaii from China and Fiji, respectively, for control are known occasionally in the Palearctic and Nearctic of the sugarcane planthopper, Perkinsiella saccharicida regions (Guglielmino et al., 2013). On the contrary, other Kirkaldy. This introduction failed, mainly because certain subfamilies, such as Anteoninae, Aphelopinae, Dryininae, hyperparasitoids of Dryinidae had been accidently and Gonatopodinae, are better known (Guglielmino and established during the preceding few years. They greatly Olmi, 2007). reduced the efficiency of the introduced dryinids. In The occurrence of 390 species of leafhoppers in Iran 1935 Aphelopus albopictus Ashmead, 1893 (=typhlocybae (Mozaffarian and Wilson, 2016) indicates the possible Muesebeck, 1935) was introduced into New Zealand from existence of many more dryinid species belonging to the United States for control of the yellow apple leafhopper different subfamilies. The genusOpsius , represented by 13 Edwardsiana crataegi (Douglas) (=Typhlocyba froggatti species in Iran, shares dryinid parasitoids also belonging to Baker). In 1994 Neodryinus typhlocybae (Ashmead, 1893) the genera Anteon Jurine, 1807 (Anteoninae); Gonatopus was introduced into Italy for the control of Metcalfa Ljungh, 1810 (Gonatopodinae); and Mirodryinus pruinosa (Say), a Nearctic planthopper pest of cultivated (Guglielmino et al., 2013). Further investigations on both plants. This introduction of N. typhlocybae was successful, salt cedar trees and other ecosystems are necessary to so the above dryinid species was introduced afterwards increase the limited knowledge of Dryinidae from Iran. in other European countries and now it is spreading Studies on the host associations of dryinids also have autonomously. At present, further programs to use significant importance in the programs for biological dryinids for biological control are under consideration in control of the leafhoppers and allied groups. Australia, Colombia, Cuba, New Zealand, Nigeria, and the United States. Acknowledgments From the point of view of efficiency as natural enemies, Special thanks to Dr Adalgisa Guglielmino (Department Gonatopodinae is the best known subfamily of Dryinidae. of Agriculture and Forestry Sciences (DAFNE), University Unluckily, Bocchinae taxa are very scarcely investigated of Tuscia, Italy) for identification of leafhopper specimens and their biology is almost unknown (Olmi, 1994). and to Dr B Nosrati (University of Zabol) for identification The knowledge on the biology of the Dryinidae is of Tamarix species. The contribution by E Rakhshani was insufficient (Olmi, 1984). The most recent reviews of the supported by Grant No. 89–9198, University of Zabol.

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