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J. Crop Prot. 2020, 9 (2): 319-325______

Research Article First record of two genera and species of Diapriinae (: ) from Iran

Mohammad Izadizadeh1, Ali Asghar Talebi1*, Victor Kolyada2, Samira Farahani3 and Ali Ameri4

1. Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran. 2. Zoological Museum of Moscow University, Moscow, Russia. 3. Research Institute of Forests and Rangelands, Agricultural Research Education and Extension Organization, Tehran, Iran. 4. Research Department, Iranian Research Institute of Plant Protection, Agricultural Research, Tehran, Iran.

Abstract: Two genera, Aneuropria Kieffer and Diapria Latreille and two species, Aneuropria foersteri (Kieffer, 1910) and Diapria conica (Fabricius, 1775) (Hymenoptera: Diapriidae) are recorded from Iran for the first time. The specimens were collected using Malaise traps from Hyrcanian forests of Mazandaran, Gulian and Golestan provinces in northern Iran. Diagnostic characters and geographical distribution of the newly recorded taxa are presented.

Keywords: Aneuropria, Diapria, Northern Iran, Hyrcanian forests,

Introduction12 Family Diapriidae includes three subfamilies: Ambositrinae Masner, 1961, Belytinae Förster, The superfamily Diaprioidea was established 1856 and Diapriinae Haliday, 1833, of which within by Masner et al. (1979); Diapriinae is largest, with 116 genera and about however, Sharkey (2007) moved Diapriidae and 1300 species (Masner and García, 2002). Species related families to a new superfamily (i.e. of the subfamily Diapriinae are solitary and Diaprioidea) based on phylogenetic study. This gregarious endoparasitoids of Diptera, especially superfamily includes four families: Diapriidae Nematocera and Cyclorrhapha. In addition, some

Downloaded from jcp.modares.ac.ir at 12:51 IRDT on Saturday May 16th 2020 Haliday, 1833, Thomson, 1858, species from Hymenoptera and Coleoptera have Monomachidae Ashmead, 1902 and been reported as hosts (Yoder, 2007). In Iran, Maamingidae Early, Masner, Naumann & nr. silvestrii (Kieffer, 1913) was Austin, 2001 (Sharkey et al., 2012), of which reported from Carpomya vesuviana Costa, 1854 Diapriidae is the most species-rich family, with (Diptera: ) (Amini et al., 2014). 2048 species reported by Huber (2017). The genus Aneuropria Kieffer, 1905 with Recently, occurrence of the family Ismaridae five species is one of the small genera of Thomson is recorded for the first time from Iran Diapriinae. From this genus, Aneuropria by a single species, rugulosus Förster, foersteri (Kieffer, 1910) and A. bifurcata 1850 (Rahmani et al., 2019). So far, the (Dodd, 1920) were reported from Palaearctic families Monomachidae and Maamingidae have region, A. kairali Rajmohana & Narendran, not been recorded from Iran. 2000 and A. nilgiriensis Sharma, 1979 from Oriental region and A. kilimandjaroi (Kieffer, 1913) from Afrotropical region (Johnson, 1992;

Notton, 2004, 2014; Rajmohana, 2006). Handling Editor: Ehsan Rakhshani ______Aneuropria foersteri is a pupal endoparasitoid * Corresponding author: [email protected] of Rhagoletis cerasi (Linnaeus, 1758) (Diptera: Received: 07 December 2019, Accepted: 10 April 2020 Tephritidae) and Piophila casei (Linnaeus, Published online: 02 May 2020

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1758) (Diptera: Piophilidae) (Thompson, 1955; Materials and Methods Teodorescu and Ursu, 1979). Diapria Latreille, 1796 is cosmopolitan Material for this study was collected from genus belonging to the subfamily Diapriinae northern area of Iran during 2010–2017 using with 25 species. Johnson (1992) listed 23 Malaise traps (Figs. 1A, B). The specimens species from different regions: Palaearctic (11 were extracted from the traps monthly, species), Oriental (four species), Nearctic (three transferred to 70% ethyl alcohol, and stored in a species), Neotropical (three species), freezer for subsequent examination. For the Australasian (one species) and Afrotropical preparation of samples, they were transferred to (one species). Later, Notton (1993) described a 96% mixture of 40% xylene and 60% alcohol, two species (i.e., Diapria cava Notton, 1993; D. moved after 2 days to amyl acetate for one day, luteipes Notton, 1993) from British Isles and finally placed on a piece of absorbing paper (England). Species of the genus Diapria are for drying (AXA method; van Achterberg, pupal endoparasitoid of Syrphidae (Diptera) 2009). The dried specimens were card-mounted (Thompson, 1955). and labeled. Illustrations were done using an Prior to this study only six species of Olympus AX70 microscope and Olympus Diapriinae were reported from Iran including: SZX9 stereomicroscope equipped with a BMZ- Coptera nr. silvestrii (Kieffer, 1913) (Amini et 04-DZ digital imaging system (Behin al., 2014), Coptera inaequalifrons (Jansson, Pajouhesh Co., Iran). A series of 4 or 5 1942), Entomacis perplexa (Haliday, 1857), captured images were merged into a single in- formosus Jansson, 1942, focus image using the image-stacking software Trichopria myrmecobia (Kieffer, 1911) and T. Combine ZP1.0. Morphological terminology longicornis (Thomson, 1858) (Samin et al., follows Nixon (1980) and Masner and Garcia 2018). So far, no data have been available on (2002). Specimens are deposited in the insect the genera Aneuropria and Diapria in Iran. collection of the Department of Entomology, Here we report two genera and two species of Tarbiat Modares University, Tehran (TMUC) this subfamily, as a part of an ongoing research and the Research Institute of Forests and on the Diapriidae fauna of Iran. Rangelands, Tehran (RIFR).

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Figure 1 Habitats of northern Iran where the specimens were collected A. Golestan, Ali Abad, Zarin Gol village, B. Mazandaran province, Alikola.

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Results Material examined: 7♀♀; Golestan, Ali Abad, Zarin Gol village (36°48′58″ N, 55°02′13″ E, The genera Aneuropria and Diapria are 694m a.s.l.), 14-V-2016, 2♀♀ (TMUC), reported from Iran for the first time, each 04.VII.2016, 2♀♀ (TMUC), 15.VII.2016, 2♀♀ represented by a single species. (RIFR), 26.VII.2016, 1♀ (TMUC). Leg. S. Genus: Aneuropria Kieffer, 1905 Farahani. Diagnosis: (Female) Body color black with Diagnosis (Female): Body length 3.3-3.4 mm; appendages lighter, predominantly smooth, head in dorsal view 1.2 times as wide as length, highly shining, with relatively little pilosity with scattered sparse hairs (Fig. 2C); eye small, some hairy cushions, but no foamy structures temple longer than length of eye (Fig. 2A), (Fig. 2A, C); Antenna 12-segmented, with postgena with cushion of hairs (Fig 2A, C); multisegmented clava; clavomeres moderately antenna clavate (Fig. 2B), scape 4.75 times as flattened ventrally, A12 longest and largest long as wide (Fig. 2B); notauli complete and segment (Fig. 2A, B); mesosoma moderately deep (Fig. 2C); pronotum and mesopleuron elongate, pronotal collar with dense hairy smooth and shiny, mesopleuron with transverse cushion; scutellum with two pits on anterior keel on lower margin; fore wing reduced, not margin; median keel of propodeum reduced; reaching beyond posterior margin of fore wing without basal and stigmal veins; propodeum (Fig. 2C); metapleuron, propodeum petiole short, about as long as wide; anterior and petiole pubescent (Fig. 2C); paired margin on 2nd tergite without notch medially longitudinal keel (plicae) on propodeum (Fig. 2C). strongly developed (Fig. 2C). Body black, Aneuropria foersteri (Kieffer, 1910) antennae and legs yellowish brown (Fig. 2A).

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Figure 2 Aneuropria foersteri (Kieffer, 1910): A. Lateral habitus of female; B. Antenna; C. Mesosoma.

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Distribution in Iran: Golestan province. often with longitudinal ridges; scutellar disc General distribution: Afrotropical, Palaearctic subrectangular, with strong median longitudinal (Denmark, Germany, Finland, Ukraine, United keel; propodeum short and hairy (Fig. 3C), with Kingdom, Russia (Johnson, 2015), Iran (New distinct median keel; wings always present, record)). submarginal vein in forewing almost straight, Biology: Endoparasitoid of Rhagoletis ceraci reaching basal third of wing, stigmal vein (Diptera: Tephritidae) (Thompson, 1955) and rudimentary, basal vein not developed; petiole Piophila casei (Diptera: Piophilidae) (Teodorescu elongate, with irregular longitudinal keels and and Ursu, 1979). abundant pilosity; anterior margin of syntergite with median notch (not straight) (Fig. 3C). Genus: Diapria Latreille, 1796 Diapria conica (Fabricius, 1775) Diagnosis: (Female) head round; postgenal Material examined: 3♀♀; Iran, Guilan cushion developed (Fig. 3A); antenna 12- province, Roodsar, Rahimabad, Ziaz segmented, with multisegmented clava (Fig. (36°52′34.44″ N, 50°13′17.40″ E, 537 m a. s. 3B); anterior margin of pronotum and l.), 29.V.2010, 2♀♀ (TMUC), Leg. M. propleuron with dense cushions (Fig. 3A); Khayrandish. Mazandaran province, Alikola mesoscutum moderately convex, with scattered (36˚13′14″ N, 53˚39′24″ E, 1626 m a.s.l.) 25- bristles; anterior scutellar pit large and deep; IV-2016, 1♀, (RIFR), Leg. S. Farahani.

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Figure 3 Diapria conica (Fabricius, 1775): A. Lateral habitus of female, B. Antenna, C. Abdomen.

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Diagnosis (Female): Body length 3.1-3.6 mm; Acknowledgments length of fore wing 2.4-2.9 mm; head in dorsal view a little wider than length (30: 28), with long We would like to thank the Department of sparse setae; antenna with five-jointed club (Fig. Entomology, Tarbiat Modares University and 3B), 6th antennal segment 2.1 times as long as Research Institute Forests and Rangelands for wide (Fig. 3B); pronotum with thick woolly providing financial support. The authors would collar; mesoscutum with two pairs of bristles; like to thank two reviewers, Dr. Ehsan Rakhshani scutellum in anterior with a deep pit and scutellar (University of Zabol) and Dr. Vasilisa G. disc with sharp keel; propodeum and petiole Chemyreva (Russian Academy of Sciences) for pubescent (Fig. 3C); petiole 1.8 times as long as their valuable comments and recommendations on wide; more than 2.0 times longer than the earlier version of this paper. its largest width (Fig. 3B), anterior margin of tergite 2 + 3 with a deep emargination (Fig. 3C); References 6th tergite longer than wide (Fig. 3C). Distribution in Iran: Guilan and Mazandaran Amini, A., Sadeghi, H., Lotfalizadeh, H. and provinces. Notton, D. 2014. Parasitoids (Hymenoptera: General distribution: North Africa, Nearctic , Diapriidae) of Carpomya and Palaearctic (Austria, Czech Republic, vesuviana Costa (Diptera: Tephritidae) in Denmark, Finland, France, Sweden, United South Khorasan province of Iran. Biharean Kingdom) (Kieffer, 1916; Kozlov, 1978; Biologist, 8(2): 122-123. Johnson, 2015). Iran (New record). Dusti, A. F. and Hayat, R. 2006. A Catalogue of Biology: of Eristalis tenax the Syrphidae (Insecta: Diptera) of Iran. (Linnaeus, 1758) (Syrphidae) (Nixon, 1980). Journal of the Entomological Research Society, 8(3): 5-38. Discussion Huber, J. T. 2017. of Hymenoptera. In: Foottit, R. G., Adler, P. H. In this study, Diapria conica and Aneuropria (Eds), Insect Biodiversity: Science and foersteri are reported for the first time from Iran. Society (2nd edn). Wiley-Blackwell, Oxford, Diapria conica is a common species and widely pp: 419-462. distributed in the Palaearctic region (Nixon, 1980; Johnson, N. F. 1992. Catalog of World species of

Downloaded from jcp.modares.ac.ir at 12:51 IRDT on Saturday May 16th 2020 Masner and García, 2002). Diapria conica is a Proctotrupoidea, exclusive of pupal parasitoid of Eristalis tenax (Linnaeus, (Hymenoptera). Memoirs of the American 1758) (Diptera: Syrphidae), which has been Entomological Institute, 51: 1-825. reported from several provinces of Iran (Dusti and Johnson, N. 2015. Fauna Europaea: Diapriidae. Hayat, 2006). The host record for A. foersteri In: Mitroiu, M.-D., Noyes, J., Cetkovic, A., includes Rhagoletis cerasi (Diptera: Tephritidae), Nonveiller, G., Radchenko, A., Polaszek, A., which is an important pest of cherry and recorded Ronquist, F., Forshage, M., Pagliano, G., from north-central and north-western provinces of Gusenleitner, J., Bartalucci, M., Olmi, M., Iran (Mohamadzadeh Namin and Korneyev, Fusu, L., Madl, M., Johnson, N., Jansta, P., 2018). Northern Iran is characterized by a great Wahis, R., Soon, V., Rosa, P., Osten, T., diversity in vegetation, natural ecosystems and Barbier, Y. and de Jong, Y. (Eds.), Fauna farm lands due to significant differences in the Europaea: Hymenoptera- (excl. topography and the varied climate (Kiani et al., ). Biodiversity Data Journal 2017). Therefore, more researches in northern and 3, e4186. [Accessed 25 November 2019]. other parts of the country are required to better Kiani, M., Mohammadi, S., Babaei, A., understand the real diversity of this large family Sefidkon, F., Naghavi, M. R., Ranjbar, M., and we expect that the Diapriidae fauna of Iran Razavi, S. A., Saeidi, K., Jafari, H., Asgari, will be substantially increased. D. and Potter, D. 2017. Iran supports a great

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share of biodiversity and floristic endemism Thomson (Hymenoptera, Diaprioidea), new to for Fritillaria spp. (Liliaceae): A review. fauna of Iran. Entomological Research, 49: Plant Diversity, 39: 245-262. 409-415. Kieffer, J. J. 1916. Diapriidae. Das Tierreich. Rajmohana, K. 2006. Studies on Proctotrupoidea Vol. 44. Walter de Gruyter and Co., Berlin, and (Hymenoptera: Insecta) 627 pp. of Kerala. Memoirs of the Zoological Survey Kozlov, M. A. 1978. Fam. . In: of India, 21(1): 1-105. Medvedev, G. S. (Ed.), A key to the Samin, N., Bagriacik, N., Turrisi, G. F., of the European Part of the USSR. Masner, L., Gençer, L., Imani, S., Lee, J. Opredelitel' nasekomykh evropeiskoi chasti W., Pujade-Villar, J. 2018. A faunistic SSSR. Nauka Publishers, Leningrad. pp. study of Chrysididae, Diapriidae, 538-664 (in Russian). , and Proctotrupidae Masner, L. and García J. L. 2002. The genera of (Hymenoptera) from Iran. Wuyi Science Diapriinae (Hymenoptera: Diapriidae) in the Journal, 34: 33-42. New World. Bulletin of the American Sharkey, M. J. 2007. Phylogeny and Museum of Natural History, 268: 1-138. classification of Hymenoptera. Zootaxa, Masner, L., Barron, J. R., Danks, H. V., 1668: 521-548. Finnamore, A. T., Francoeur, A., Gibson, G. Sharkey, M. J., Vilhelmsen, L., Heraty, J., A. P., Mason, W. R. M. and Yoshimoto, C. Liljeblad, J., Dowling, A. P. G., M. 1979. Hymenoptera. In: Danks, H. V. Schulmeister, S., Murray, D., Deans, A. R., (Ed.), Canada and its Insect Fauna. Memoirs Ronquist, F., Krogmann, L. and Wheeler, of the Entomological Society of Canada No. W. C. 2012. Phylogenetic relationships 108: 485-508. among superfamilies of Hymenoptera. Mohamadzadeh Namin, S. and Korneyev, V. A. Cladistics, 28: 80-112. 2018. An annotated checklist of fruit Teodorescu, I. and Ursu, A. 1979. [Species of (Diptera: Tephritidae) of Iran. Zootaxa, Diapriinae (Hymenoptera-Proctotrupoidea), 4369(3): 377-405. puparia parasites of synantropic Diptera]. Nixon, G. E. J. 1980. Diapriidae (Diapriinae). Studii si Cercetari de Biologie Seria Hymenoptera, Proctotrupoidea. Handbooks for Biologie Animala, 31: 131-136. the Identification of British insects, 8(3): 1-55. Thompson, W. R. 1955. A catalogue of the

Downloaded from jcp.modares.ac.ir at 12:51 IRDT on Saturday May 16th 2020 Notton D. G. 1993. New species of Trichopria parasites and predators of insect pests. and Diapria from the British Isles (Hym., Section 2. Host parasite catalogue, Part 3. Proctotrupoidea, Diapriidae). Entomologist’s Hosts of the Hymenoptera (Calliceratid to Monthly Magazine, 129: 139-149. Evaniid). Commonwealth Agricultural Notton, D. G. 2004. A catalogue of types of Bureaux, The Commonwealth Institute of Diapriinae (Hymenoptera, Diapriidae) at the Biological Control, Ottawa, Ontario, National Museum of Natural History, Paris, Canada. with notes on the classification of Diapriinae van Achterberg, C. 2009. Can Townes type and a brief history of the types of Jean- Malaise traps be improved? Some recent Jacques Kieffer (1856-1925). Zoosystema, developments. Entomologische Berichten 26(2): 315-352. Amsterdam, 69(4): 129-135. Notton, D. G. 2014. A catalogue of the types of Yoder, M. J. 2007. Advances in diapriid Diapriinae (Hymenoptera, Diapriidae) at the (Hymenoptera: Diapriidae) systematics, with Natural History Museum, London. European contributions to cybertaxonomy and the Journal of Taxonomy, 75: 1-123. analysis of rRna sequence data. Dissertation Rahmani, Z., Kim, C. J., Ghafouri Moghaddam, (Doctor of Philosophy)-Texas A & M M. and Rakhshani, E. 2019. Family Ismaridae University. 185 pp.

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اوﻟﯿﻦ ﮔﺰارش دو ﺟﻨﺲ و ﮔﻮﻧﻪ از زﻧﺒﻮرﻫﺎي زﯾﺮﺧﺎﻧﻮاده (Diapriinae (Hymenoptera: Diapriidae از اﯾﺮان

ﻣﺤﻤﺪ اﯾﺰديزاده1، ﻋﻠﯽاﺻﻐﺮ ﻃﺎﻟﺒﯽ1*، وﯾﮑﺘﻮر ﮐﻮﻟﯿﺎدا2، ﺳﻤﯿﺮا ﻓﺮاﻫﺎﻧﯽ3 و ﻋﻠﯽ ﻋﺎﻣﺮي4

1- ﮔﺮوه ﺣﺸﺮهﺷﻨﺎﺳﯽ ﮐﺸﺎورزي، داﻧﺸﮑﺪه ﮐﺸﺎورزي، داﻧﺸﮕﺎه ﺗﺮﺑﯿﺖ ﻣﺪرس، ﺗﻬﺮان، اﯾﺮان. 2- ﻣﻮزه ﺟﺎﻧﻮرﺷﻨﺎﺳﯽ داﻧﺸﮕﺎه ﻣﺴﮑﻮ، ﻣﺴﮑﻮ، روﺳﯿﻪ. 3- ﻣﺆﺳﺴﻪ ﺗﺤﻘﯿﻘﺎت ﺟﻨﮕﻞﻫﺎ و ﻣﺮاﺗﻊ، ﺳﺎزﻣﺎن ﺗﺤﻘﯿﻘﺎت، ﺗﺮوﯾﺞ و آﻣﻮزش ﮐﺸﺎورزي، ﺗﻬﺮان، اﯾﺮان. 4- ﺑﺨﺶ ﺗﺤﻘﯿﻘﺎت ردهﺑﻨﺪي، ﻣﺆﺳﺴﻪ ﺗﺤﻘﯿﻘﺎت ﮔﯿﺎهﭘﺰﺷﮑﯽ ﮐﺸﻮر، ﺳﺎزﻣﺎن ﺗﺤﻘﯿﻘﺎت، ﺗﺮوﯾﺞ و آﻣﻮزش ﮐﺸﺎورزي، ﺗﻬﺮان، اﯾﺮان. ﭘﺴﺖ اﻟﮑﺘﺮوﻧﯿﮑﯽ ﻧﻮﯾﺴﻨﺪه ﻣﺴﺌﻮل ﻣﮑﺎﺗﺒﻪ: [email protected] درﯾﺎﻓﺖ: 15 ﻣﻬﺮ 1398؛ ﭘﺬﯾﺮش: 22 ﻓﺮوردﯾﻦ 1399

ﭼﮑﯿﺪه: دو ﺟـﻨﺲ Diapria و Aneuropria و دو ﮔﻮﻧـﻪ (Aneuropria foersteri (Kieffer, 1910 و Diapria (Hymenoptera: Diapriidae) conica (Fabricius, 1775) ﺑﺮاي اوﻟﯿﻦ ﺑﺎر از اﯾﺮان ﮔﺰارش ﻣـﯽ ﺷـﻮ ﻧﺪ. ﻧﻤﻮﻧـﻪ ﻫـﺎ ﺑﻪوﺳﯿﻠﻪ ﺗﻠﻪ ﻣﺎﻟﯿﺰ از اﺳﺘﺎن ﻫﺎي ﻣﺎزﻧﺪران، ﮔﻠﺴﺘﺎن و ﮔـﯿﻼن ﺟﻤـﻊ آوري ﺷـﺪﻧﺪ . ﺧـﺼﻮﺻﯿﺎت اﻓﺘﺮاﻗـﯽ و اﻧﺘـﺸﺎر ﺟﻐﺮاﻓﯿﺎﯾﯽ ﺟﻨﺲﻫﺎ و ﮔﻮﻧﻪﻫﺎ اراﯾﻪ ﺷﺪ.

وازﮔﺎن ﮐﻠﯿﺪي: Diapria ،Aneuropria، ﻣﺎزﻧﺪران، ﮔﻠﺴﺘﺎن، ﮔﯿﻼن، ﺟﻨﮕﻞﻫﺎي ﻫﯿﺮﮐﺎﻧﯽ، ﭘﺎرازﯾﺘﻮﯾﯿﺪ Downloaded from jcp.modares.ac.ir at 12:51 IRDT on Saturday May 16th 2020

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