Turkish Journal of Zoology Turk J Zool (2015) 39: 1121-1131 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1402-61

New host and new records of Charipinae (Hymenoptera: Cynipoidea: Figitidae) from

1, 2 3 3 1 Mar FERRER-SUAY *, Jesús SELFA , Ehsan RAKHSHANI , Elham NADER , Juli PUJADE-VILLAR 1 Department of Animal Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain 2 Department of Zoology, Faculty of Biological Sciences, University of Valencia, Burjassot-Paterna Campus, Burjassot, Spain 3 Department of Plant Protection, College of Agriculture, University of Zabol, Zabol, Iran

Received: 27.02.2014 Accepted/Published Online: 05.09.2015 Printed: 30.11.2015

Abstract: Charipinae material collected from various localities in Iran was studied. A total of 712 specimens have been determined in 8 species: Alloxysta arcuata (Kieffer, 1902), A. brevis (Thomson, 1862), A. circumscripta (Hartig, 1841), A. citripes (Thomson, 1862), A. darci (Girault, 1933), A. mullensis (Cameron, 1883), A. pusilla (Kieffer, 1902), and Phaenoglyphis villosa (Hartig, 1841). Alloxysta circumscripta and A. darci are cited for the first time from Iran. In total, 91 host associations (Charipinae-Aphidiinae-Aphid-host plant) are recorded, of which 23 are new to science. New trophic relationships are also recorded for Iran for A. brevis, A. mullensis, and P. villosa. Diagnoses, short descriptions, and figures are included for the newly recorded species.

Key words: Figitidae, Charipinae, Alloxysta, Phaenoglyphis, Iran

1. Introduction The Charipinae fauna from Iran has been recently Members of the subfamily Charipinae are very small wasps revised (Ferrer-Suay et al., 2013e). Fifteen species were (0.8–2.0 mm), characterized by having a smooth and shiny identified in that work, 9 of which were recorded for body. The morphological features of these small wasps the first time from this region. They included Alloxysta are much reduced, and for this reason the identification arcuata (Kieffer, 1902), A. brevis (Thomson, 1862), A. at species level is a very difficult task. On the other hand, castanea (Hartig, 1841), A. macrophadna (Hartig, 1841), the Charipinae are a biologically important group, being A. melanogaster (Hartig, 1840), A. pusilla (Kieffer, 1902), secondary parasitoids of aphids (Hemiptera: Aphididae) via A. ruficollis (Cameron, 1883), A. tscheki (Giraud, 1860), Aphidiinae (Hymenoptera: Braconidae) and Aphelininae and A. ullrichi (Giraud, 1860). Later, A. ramulifera (Hymenoptera: Braconidae), and secondary parasitoids (Thomson, 1862) was also recorded for the first time from of psyllids (Hemiptera, Psylloidea) via Encyrtidae Iran (Ferrer-Suay et al., 2013d). (Hymenoptera: Chalcidoidea) (Menke and Evenhuis, 1991). The objective of the present work was to study The biological importance of the Charipinae lies in additional material that was recently collected from their lifestyle. As secondary parasitoids of aphids, they various habitats in 4 central and eastern . have an influence on the aphids’ and primary parasitoids’ Trophic relationships are also recorded for the collected abundance. According to van Veen et al. (2001), secondary species. Diagnoses, short descriptions, and figures are parasitoids can reduce the efficiency of primary parasitoids included for the newly recorded species. on their hosts in at least 3 ways: (i) increasing primary parasitoids’ mortality; (ii) increasing the growth rate of 2. Materials and methods the aphid population indirectly; and (iii) increasing the Collection of specimens was performed mainly in propensity for primary parasitoids to disperse. Charipinae (central) and North Khorasan (northeastern) provinces by hyperparasitoids influence the effectiveness of the primary rearing host aphids, and in Khorasan Razavi and Sistan parasitoids of aphids by decreasing their abundance and and Baluchestan provinces using a standard sweeping net modifying their behavior. As a result, the increase of aphid during 2007–2011. The plant material bearing the aphid populations can cause severe yield losses in some crops colonies was gently cut, directly placed within transparent (Ferrer-Suay et al., 2012a). plastic boxes, and covered with mesh for ventilation. The * Correspondence: [email protected] 1121 FERRER-SUAY et al. / Turk J Zool samples were subsequently transferred to the laboratory, 3. Results where they were subdivided, with part used to obtain Among the 712 examined specimens, there were 8 voucher aphids for identification and another part held Charipinae species in association with 19 Aphidiinae for rearing the parasitoids and hyperparasitoids. The parasitoids and 16 aphid species. In total, 91 host boxes were kept at room temperature (within a range of associations (Charipinae-Aphidiinae-aphid-host plant) 22 ± 5 °C) until emergence of the adult parasitoids and were recorded, of which 23 are new to science. Recorded hyperparasitoids. The emerged specimens were captured species are listed below alphabetically. For each species, the twice per day using an aspirator to avoid further parasitic list of material examined, including Aphidiinae primary activities inside the rearing boxes. Captured specimens parasitoid, host aphid on host plant, locality date, number were directly dropped into 75% ethanol for preservation of specimens, and name of legator is provided. and identification at later steps. Alloxysta arcuata (Kieffer, 1902) The external morphology of Charipinae specimens Allotria (Allotria) arcuata Kieffer, 1902: 12. Type: was studied using a stereomicroscope (NIKON SMZ-1) BMNH (examined). and an environmental scanning electron microscope (FEI Material examined. (64♂ and 68♀). “Lysiphlebus Quanta 200 ESEM). The field-emission gun environmental fabarum – Aphis fabae on Beta vulgaris, Isfahan-Jafarabad, scanning electron microscope was used for high-resolution 11-ix-2010”: 4♂ and 2♀; “Diaeretiella rapae, Binodoxys imaging without gold-coating the specimens. For each acalephae – Aphis fabae on Phaseolus vulgaris, Isfahan- new record for Iran, a diagnosis and short description have Flavarjan, 05-xi-2010”: 1♂; “Aphis fabae on Circium been added. vulgare, Isfahan-Fereydonshahr, 04-vi-2011”: 5♂ and 3♀; Type material of the species studied is deposited in the “Lysiphlebus fabarum – Aphis fabae on Ononis spinosa, ♀ following institutions: Isfahan-Jafarabad, 20-v-2011”: 1 ; “Cucumis sativus, Isfahan-Jafarabad, 11-ix-2010”: 2♂ and 1♀; “Lysiphlebus - BMNH: Natural History Museum (London, United fabarum – Aphis craccivora Koch on Robinia pseudoacacia, Kingdom). Isfahan-Najvan, 25-iv-2011”: 2♂ and 10♀; “Lysiphlebus - MZLU: Lund Museum of Zoology (Lund, Sweden). fabarum – Aphis craccivora on Sophora mollis, Isfahan- - NHMA: Natural History Museum (Amiens, France). Dourche, 15-iv-2011”: 2♂ and 5♀; “Lysiphlebus fabarum, - QM: Queensland Museum (Brisbane, Australia). Aphidius matricariae Haliday – Aphis craccivora on - ZSM: Zoologische Staatssammlung Museum (Munich, Medicago sativa, Isfahan-Dourche, 15-iv-2011”: 8♂ Germany). and 4♀; “Aphidius matricariae, Binodoxys acalephae – Morphological terms used are taken from Paretas- Aphis craccivora on Trifolium repens Isfahan-Isfahan”: Martínez et al. (2007). Measurements and abbreviations 5♂; “Binodoxys acalephae – Aphis fabae on Phaseolus include F1–F12, first and subsequent flagellomeres. The vulgaris, Isfahan-Isfahan”: 1♀; “Lysiphlebus fabarum – width of the forewing radial cell is measured from the Brachycaudus tragopogonis (Kaltenbach) on Tragopogon margin of the wing to the beginning Rs vein. The transfacial graminfolius, Isfahan-Goldasht,14-iv-2011”: 15♂ and line is measured as the distance between the inner margins 19♀; “Lysiphlebus fabarum – Aphis craccivora on Robinia of the compound eyes, measured across the face through pseudoacacia, Isfahan-Dourche, 15-iv-2011”: 2♀; the antennal toruli, divided by the height of the eye. The “Lysiphlebus fabarum – Aphis rubiae Narzikulov on Rubia malar space is measured by the distance from the lower tinctorum, Isfahan-Isfahan”: 3♂ and 1♀; “Praon volucre part of the gena from the mouthparts to the ventral (Haliday) – Aphis fabae on Phaseolus vulgaris, Isfahan- margin of the compound eye, divided by the height of the Najvan, 17-ix-2010”: 10♂ and 4♀; “Binodoxys acalephae eye. Females and males of the species shortly described – Aphis fabae on Phaseolus vulgaris, Isfahan-Najvan, 10- have the same characters except where indicated. Aphid x-2010”: 1♂ and 4♀; “Lysiphlebus fabarum – Aphis fabae nomenclature follows Remaudiére and Remaudiére (1997). on Phaseolus vulgaris, Isfahan-Filour, 03-ix-2010”: 3♂ and Aphid slides and Aphidiinae specimens are deposited 5♀; “Lysiphlenus fabarum – Aphis fabae on Chenopodium in the insect collection of the Faculty of Agriculture, album, Isfahan-Dourche, 21-v-2009”: 2♂ and 4♀, Leg. E. University of Zabol, Iran (FAUOZ). Charipinae species Nader; “Lysiphlebus fabarum – Brachycaudus tragopogonis are deposited in the University of Barcelona (UB) (Pujade- on Tragopogon gramnifolius, North Khorasan-Shirvan, 25- Villar collection). World host range has been included in vi-2007, Leg. S. Kazemzadeh”: 1♂ and 2♀. the host section of each determined species. Host data are Distribution. Cosmopolitan. listed as follows: HP: host plant; HA: host aphid; HS: host Hosts. HP: unknown, HA: Myzus cerasi, HW: unknown psyllid; HW: primary host parasitoid (wasp); when any of (Ionescu, 1969: 268); HP: Ligustrum ovalifolium, HA: these categories is not known, “unknown” is inserted into Myzus ligustri, HW: unknown (Evenhuis, 1976: 143); HP: the corresponding trophic level. unknown, HA: unknown, HW: Ephedrus sp., Ephedrus

1122 FERRER-SUAY et al. / Turk J Zool persicae (Evenhuis and Barbotin, 1977: 189). HP: Lilium 37♂ and 27♀; “Diaeretiella rapae, Aphidius matricariae – sp., HA: Macrosiphum sp., HW: unknown; HP: Canna Aphis gossypii on Solanum melongena, Isfahan-Hoye, 18- sp., HA: Macrosiphum euphorbiae, HW: unknown; HP: vii-2009”: 5♂ and 2♀; “Praon sp., Lysiphlebus fabarum – unknown, HA: Aphis fabae, HW: unknown; HP: Zea mays, Aphis solanella on Chenopodium album, Isfahan-Dourche, HA: Rhopalosiphum padi, HW: unknown; HP: Bromus sp., 01-vi-2009”: 5♂ and 4♀; “Binodoxys acalephae – Aphis HA: Rhopalosiphum padi, HW: Lysiphlebus testaceipes; HP: fabae on Phaseolus vulgaris, Isfahan-Najvan, 10-x-2010”: Cassia sp., HA: Aphis gossypii, HW: unknown; HP: Zea 1♂ and 1♀; “Lysiphlebus fabarum – Aphis craccivora on mays, HA: Rhopalosiphum padi, HW: unknown; HP: Citrus Medicago sativa, Isfahan-Najvan, 25-iv-2011”: 1♂ and 3♀; limon, HA: unknown, HW: unknown; HP: unknown, HA: “Lysiphlebus fabarum – Aphis fabae on Phaseolus vulgaris, Myzus persicae, HW: unknown; HP: Jacaranda sp., HA: Isfahan-Filour, 03-ix-2010”: 2♀; “Lysiphlebus fabarum – Aphis gossypii, HW: unknown; HP: Populus tremuloides, Aphis fabae on Chenopodium album, Isfahan-Dourche, HA: Chaitophorus sp., HW: unknown; HP: Nerium 21-v-2009”: 1♂ and 1♀, Leg. E. Nader. oleander, HA: Aphis nerii, HW: unknown; HP: Malva sp., Distribution. Cosmopolitan. HA: Aphis sp., HW: unknown; HP: unknown, HA: Aphis Hosts. HP: Lycopersicum esculentum, HA: unknown, gossypii, HW: Lysiphlebus testaceipes; HP: Iris sp., HA: HW: unknown (Dalla Torre and Kieffer, 1910: 290). HP: Dysaphis sp., HW: unknown; HP: unknown, HA: Myzus Populus trichocarpa, HA: Chaitophorus populicola Thomas, persicae, HW: unknown; HP: unknown, HA: Mentha HW: Aphelinus sp. (Andrews, 1978: 68). HP: unknown, piperita var. citrata, HW: unknown; HP: unknown, HA: HA: Myzus persicae, HW: Diaeretiella rapae and Aphidius Mentha pulegium, HW: unknown; HP: unknown, HA: sp. (Horn 1984: 19). HP: unknown, HA: Aphis sp., HW: Mentha spicata var. tashkent, HW: unknown (Ferrer-Suay Lysephedrus sp.; HP: unknown, HA: Myzus cerasi and et al., 2013a: 30). Dysaphis plantaginea, HW: Ephedrus persicae (Fergusson Alloxysta brevis (Thomson, 1862) 1986: 18). HP: unknown, HA: Aphis sp., HW: Lysephedrus Allotria brevis Thomson, 1862: 408. Type: MZLU sp.; HP: unknown, HA: Myzus cerasi and Dysaphis (examined). plantaginea, HW: Ephedrus sp. (Barczak, 1991: 92). HP: Material examined. (68♂ and 80♀). “Lysiphlebus unknown, HA: Hyperomyzus lactucae, HW: Praon volucre fabarum – Aphis fabae on Beta vulgaris, Isfahan-Jafarabad, (Tizado and Nuñez-Perez, 1993: 97). HP: unknown, HA: 11-ix-2010”: 1♀; “Diaeretiella rapae, Binodoxys acalephae – Eucallipterus tiliae, HW: Trioxys curvicaudus and Trioxys Aphis fabae on Phaseolus vulgaris, Isfahan-Flavarjan, 05-xi- tenuicaudus (Zuparko and Dahlsten, 1995: 730). HP: 2010”: 3♂ and 2♀; “Cucumis sativus, Isfahan-Jafarabad, 11- Citrus sp., HA: Toxoptera citricidus, HW: Lysiphlebus ix-2010”: 1♀; “Lysiphlebus fabarum, Aphidius matricariae testaceipes (Evans and Stange, 1997: 1). HP: unknown, – Aphis craccivora on Medicago sativa, Isfahan-Dourche, HA: Capitophorus carduinus and Sitobion sp. (Müller et 15-iv-2011”: 4♀; “Aphis fabae on Phaseolus vulgaris, al., 1999: 346). HP: Euonymus europaea, HA: Aphis fabae, Isfahan-Flavarjan, 05-xi-2010”: 1♀; “Aphidius matricariae, HW: Binodoxys angelicae (Hübner et al., 2002: 508). HP: Lysiphlebus fabarum – Aphis umbrella on Malva sylvestris, Solidago altissima, HA: Uroleucon nigrotuberculatum, Isfahan-, 06-vi-2011”: 1♀; “Adialytus ambiguus HW: Aphelinus albipodus (Takada and Nakamura, 2010: – Sipha elegans on Gastridium phleoides, Isfahan-Najvan, 270). HP: Cassia sp., HA: Aphis gossypii, HW: unknown; 09-v-2011”: 1♀; “Lysiphlebus fabarum – Aphis origani HP: Yucca sp., HA: Aphis helianthi Monell, HW: unknown on Mentha longifolia, Isfahan-Varposht, 26-v-2011”: (Ferrer-Suay et al., 2013a: 32). 1♀; “Aphidius matricariae, Binodoxys acalephae – Aphis Comments. Alloxysta brevis is here recorded for the craccivora on Trifolium repens, Isfahan-Isfahan,”: 1♂ and first time in association with Binodoxys acalephae and 5♀; “Aphidius matricariae, Lysiphlebus fabarum – Aphis Aphidius matricariae. craccivora on Trifolium campestre, Isfahan-Isfahan”: 3♂ Alloxysta circumscripta (Hartig, 1841) (Figures 1a–1d) and 1♀; “Adialytus salicaphis (Fitch) – Chaitophorus Xystus circumscriptus Hartig, 1841: 352. Type: ZSM sp. on Populus alba, Isfahan-, 13-xi-2010”: (examined). 1♂; “Diaeretiella rapae, Aphidius matricariae – Aphis Material examined: (17♂ and 18♀). “Praon yomenae, sp. on Brassicaceae host plant, Isfahan-Dourche, 15-iv- Ephedrus niger – Uroleucon sp. on Acroptilon repens, 2011”: 1♀; “Lysiphlebus fabarum – Aphis rubiae on Rubia Isfahan-Filour, 09-iv-2011”: 17♂ and 18♀; “Praon tinctorum, Isfahan-Isfahan”: 8♂ and 20♀; “Binodoyxs yomenae, Aphidius persicus – Uroleucon sonchi (L.) acalephae – Aphis fabae on Phaseolus vulgaris, Isfahan- on Sonchus oleraceus, Isfahan-Najafabad, 29-x-2010”: Hoye, 15-x-2010”: 1♂; “Aphidius matricariae – Aphis 1♂; “Uroleucon sonchi on Sonchus oleraceus, Isfahan- solanella Theobald on Solanum melongena, Isfahan- Najafabad, 07-vii-2010”: 1♀, Leg. E. Nader. Najvan, 10-x-2010”: 1♂ and 1♀; “Praon volucre – Aphis Diagnosis. Alloxysta circumscripta is mainly fabae on Phaseolus vulgaris, Isfahan-Najvan, 17-ix-2010”: characterized by having a closed radial cell being 2.3 times

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Figure 1. Diagnostic features of Alloxysta circumscripta: a) radial cell; b) antenna; c) pronotum; d) propodeum. as long as wide (Figure 1a), pronotal carinae present (Figure than remaining flagellomeres, F3–F11 with rhinaria and 1c), propodeal carinae absent (Figure 1d), female antennae club-shaped; F1 longer than pedicel and F2, F2 shorter with the beginning of rhinaria in F5, F2 shorter than F3, then F3, F3 shorter than F4 (Figure 1b). Male antennae F3 shorter than F4 (Figure 1b), male antennae with the 14-segmented; F1–F3 smooth and thinner than remaining beginning of rhinaria in F4, F2 longer than F3, F3 shorter flagellomeres, F4–F12 with rhinaria and club-shaped; F1– than F4. It is similar to A. consobrina (Zetterstedt, 1838), F3 straight; F1 longer than pedicel and F2, F2 longer than but they can be differentiated by the proportions between F3, and F3 shorter than F4. Pronotum covered by many flagellomeres: F1 subequal to F2, F2 shorter or subequal to setae with 2 carinae clearly present under the pubescence F3 in A. circumscripta (Figure 1b) while F1 longer than F2, (Figure 1c). Propodeum also covered by abundant setae, F2 subequal to F3 in A. consobrina (Zetterstedt, 1838); size without carinae present (Figure 1d). Forewing longer than of radial cell: 2.3 times as long as wide in A. circumscripta body; radial cell partially open, 2.3 times as long as wide (Figure 1a) but 2.7 times as long as wide in A. consobrina. (Figure 1a). Short description. Head, mesosoma, and metasoma Distribution. Andorra (Ferrer-Suay et al., 2011a: 354); dark brown; scape, pedicel, F1, and F2 yellow, F3–F12 Austria (Giraud, 1860: 127; Hellén, 1963: 17); England yellowish brown; legs yellow and veins yellowish brown. (Dalla Torre and Kieffer, 1910: 278; Müller et al., 1999: Female antennae 13-segmented; F1–F2 smooth, thinner 346); Finland (Hellén, 1963: 17); France (De Gaulle, 1908:

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26); Germany (Hartig, 1841: 352); Poland (Kierych, 1979: Diagnosis. Alloxysta darci is mainly characterized by 15); Scotland (Cameron, 1886: 86). New record from Iran. having small closed radial cell, being 2.4 times as long Host. HP: Raphanus sp., HA: Aphis sp., HW: unknown as wide (Figure 2a), pronotal carinae absent (Figure 2b), (Giraud, 1877: 416). HP: Fennel sp., HA: Aphis sp., HW: propodeal plate present (Figure 2d), rhinaria and club unknown; HP: Chaerophyllum sylvestre, HA: Cinara pini shape begin in F4, F1 shorter than pedicel, and antennae (L.), Cryptomyzus ribis (L.), and Aphis sambuci (L.) (De longer than body length in both male and female (Figure Gaulle, 1908: 26; Dalla Torre and Kieffer, 1910: 277). 2c). This species is similar to A. brevis, but they can be HP: unknown, HA: Uroleucon sp., HW: Praon dorsale differentiated by the antennae length: longer than body in (Haliday) auct. (Evenhuis, 1982: 22). HP: unknown, HA: A. darci, while shorter in A. brevis; forewing with marginal Acyrthosiphon pisum (Harris), HW: Praon sp. (Müller et setae longer in A. darci, while they are shorter in A. brevis. al., 1999: 352). Short description. Head yellowish brown, mesosoma Comments. Alloxysta circumscripta is here recorded and metasoma brown; scape, pedicel, F1–F3 yellow, for the first time in association with Praon yomenae, rest of flagellomeres brown; legs yellowish; veins Ephedrus niger, and Aphidius persicus. yellowish brown. Female antennae 13-segmented; F1–F3 Alloxysta citripes (Thomson, 1862) smooth and thinner than remaining ones; F4–F11 with Allotria citripes Thomson, 1862: 410. Type: MZLU rhinaria and club shape; F1 shorter than pedicel, F1–F3 (examined). subequal, F3 shorter than F4 (Figure 2c). Male antennae Material examined. (18♂ and 20♀). “Trioxys pallidus 14-segmented; F1–F3 smooth and thinner than remaining – Chromaphis juglandicola on Juglans regia, Isfahan- ones; F4–F12 with rhinaria and club shape, with the same Najafabad, 02-v-2011”: 1♂ and 2♀; “Trioxys pallidus proportions between flagellomeres as female. Pronotum – Chromaphis juglandicola on Juglans regia, Isfahan- covered with setae with few setae on distolateral corners, Mohamadiye, 20-v-2011”: 1♂ and 3♀; “Trioxys pallidus without carinae present (Figure 2b). Propodeum covered – Chromaphis juglandicola on Juglans regia, Isfahan-Hoye, by abundant pubescence; 2 wide carinae present forming 15-v-2011”: 11♂ and 9♀; “Trioxys pallidus – Chromaphis a plate, separated by a few setae on first third and forming juglandicola on Juglans regia, Isfahan-Varposht, 28- a plate on last two-thirds; sides subparallel anteriorly and v-2011”: 4♂ and 4♀; “Trioxys pallidus – Chromaphis very slightly curved posteriorly (Figure 2d). Forewing juglandicola on Juglans regia, Isfahan-Najafabad, 29-v- longer than body, radial cell closed, 2.4 times as long as 2011”: 1♂ and 2♀, Leg. E. Nader. wide in both sexes (Figure 2a). Distribution. Holarctic, Neotropic, and African Distribution. Species known from the Palearctic and (Ferrer-Suay et al., 2012a). the Australian region (Ferrer-Suay et al., 2012a). Spain Host. HP: unknown, HA: Eucallipterus tiliae, HW: (Ferrer-Suay et al., 2013c: 323). New record from Iran. unknown (De Gaulle, 1908: 26). HP: unknown, HA: Host. HP: unknown, HA: Aphis craccivora and Dysaphis mali, HW: unknown (Belizin, 1966: 6). HP: Hyalopterus pruni (Geoffroy), HW: Aphelinus flaviventris Quercus sp., HA: Tuberculoides annulatus, HW: unknown; Kurdjumov; HP: unknown, HA: Macrosiphum euphorbiae, HP: Alnus glutinosa, HA: Pterocallis alni, HW: unknown; HW: Aphelinus gossypii Timberlake; HP: unknown, HA: HP: Corylus avellana, HA: Myzocallis coryli, HW: unknown; Myzus persicae, HW: Aphelinus gossypii; HP: unknown, HP: unknown, HA: unknown, HW: Trioxys pallidus HA: unknown, HW: Aphelinus varipes (Förster) (Carver, (Evenhuis, 1976: 140). HP: unknown, HA: Tuberculoides 1992: 770). HP: Sorghum bicolor, HA: Rhopalosiphum sp., Pterocallis sp., and Myzocallis sp., HW: Trioxys sp.; maidis (Fitch), HW: Aphelinus varipes. HP: unknown, HA: Drepanosiphum sp., HW: Aphelinus Alloxysta mullensis (Cameron, 1883) sp. (Fergusson, 1986: 18). HP: unknown, HA: Eucalipterus Allotria mullensis Cameron, 1883: 366. Type: BMNH tiliae, HW: unknown (Evenhuis and Barbotin, 1987: 214). (examined). HP: Tilia cordata, HA: Eucallipterus tiliae, HW: Trioxys Material examined. (3♂ and 16♀). “Lysiphlebus pallidus (Hübner et al., 2002: 508). HP: Juglans regia, HA: fabarum – Aphis fabae on Circium vulgare, Isfahan- Chromaphis juglandicola, HW: unknown (Ferrer-Suay et Fereydonshahr, 04-vi-2011”: 4♀; “Lysiphlebus fabarum al., 2012c: 10). – Aphis fabae on Ononis spinosa, Isfahan-Jafarabad, 20-v- Alloxysta darci (Girault, 1933) (Figures 2a–2d) 2011”: 2♀; “Aphidius matricariae, Lysiphlebus fabarum – Allotria d’arci Girault, 1933: 2. Type: QM (examined). Aphis umbrella on Malva sylvestris, Isfahan-Najafabad, 06- Material examined: (6♂ and 2♀). “Swept on Medicago vi-2011”: 1♀; “Aphidius matricariae, Binodoxys acalephae sativa, Khorasan Razavi-Sabzevar-Joghatay, 08-ix-2011”: – Aphis craccivora on Trifolium repens, Isfahan-Isfahan,”: 5♂ and 1♀, Leg. Kh. Fathabadi; “Swept on Medicago 1♂ and 1♀; “Trioxys pallidus – Chromaphis juglandicola sativa, Sistan & Baluchestan-Zabol, 09-vi-2011”: 1♂ and on Juglans regia, Isfahan-Varposht, 28-v-2011”: 1♂ and 1♀, Leg.: F. Goli-Mahmoudi. 1♀; “Lysiphlebus fabarum – Aphis fabae and Brachycaudus

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Figure 2. Diagnostic features of Alloxysta darci: a) fore wing; b) pronotum; c) antenna; d) propodeum. cardui (L.) on Circium arvense, Isfahan-Varposht, 28-v- Ephedrus sp. (Bokina, 1997: 435). HP: Brassica oleracea, 2011”: 1♂; “Lysiphlebus fabarum – Aphis craccivora on HA: unknown, HW: unknown (Ferrer-Suay et al., 2013a: Robinia pseudoacacia, Isfahan-Dourche, 15-iv-2011”: 37). 3♀; “Aphidius matricariae, Lysiphlebus fabarum – Aphis Comments. Alloxysta mullensis is here recorded for the craccivora on Trifolium campestre, Isfahan-Isfahan”: 1♀; first time in association with Binodoxys acalephae. “Diaeretiella rapae, Aphidius matricariae – Aphis sp. on Alloxysta pusilla (Kieffer, 1902) Brassicaceae host plant, Isfahan-Dourche, 15-iv-2011”: Allotria (Allotria) pusilla Kieffer, 1902: 13. Type: 1♀; “Lysiphlebus fabarum – Aphis fabae on Phaseolus NHMA. vulgaris, Isfahan-Filour, 03-ix-2010”: 2♀. Material examined. (1♂). “Lysiphlebus fabarum – Distribution. Cosmopolitan, except for Australia and Aphis fabae on Ononis spinosa, Isfahan-Jafarabad, 20-v- Oriental regions (Ferrer-Suay et al., 2012a). 2011”: 1♂, Leg. E. Nader. Host. HP: Urtica dioica, HA: Aphis urticata, HW: Distribution. Palearctic and Neotropic (Ferrer-Suay et Lysiphlebus fabarum; HP: Philadelphus coronarius, HA: al., 2012a). Aphis fabae, HW: Lysiphlebus fabarum (Evenhuis, 1978: Host. HP: Chrysanthemum leucanthemum, Salix 173). HP: unknown, HA: unknown, HW: Praon sp. and viminalis and Populus alba, HA: Aphis sp., HW: unknown

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(Kieffer, 1902: 13). HP: Chrysanthemum sp., Populus sp. and “Diaeretiella rapae, Aphidius matricariae – Aphis sp. on Salix sp., HA: Aphis sp., HW: unknown (De Gaulle, 1908: Brassicaceae host plant, Isfahan-Dourche, 15-iv-2011”: 1♀; 26). HP: Cirsium arvense, HA: Aphis fabae cirsiiacanthoidis “Diaeretiella rapae, Lysiphlebus fabarum – Aphis craccivora Scopoli, HW: Lysiphlebus cardui (Marshall) (Hübner et al., on Cardaria draba, Isfahan-Dourche, 15-iv-2011”: 7♂ and 2002: 509). 1♀; “Praon yomenae, Aphidius persicus – Uroleucon sonchi Phaenoglyphis villosa (Hartig, 1841) on Sonchus oleraceus, Isfahan-Najafabad, 29-x-2010”: 1♂; Xystus villosus Hartig, 1841: 353. Type: ZSM “Praon rosaecola, Aphidius rosae – Macrosiphum rosae (examined). on Rosa sp. Isfahan-Najvan, 10-x-2010”: 4♀; “Aphidius Material examined. (118♂ and 152♀). “Lysiphlebus matricariae – Aphis gossypii on Solanum melongena, fabarum – Aphis craccivora on Amaranthus retroflexus, Isfahan-Najvan, 10-x-2010”: 1♀; “Praon volucre – Aphis Isfahan-Najvan, 17-ix-2010”: 2♀; “Diaeretiella rapae, fabae on Phaseolus vulgaris, Isfahan-Najvan, 17-ix- Binodoxys acalephae – Aphis fabae on Phaseolus vulgaris, 2010”: 2♂ and 2♀; “Binodoxys acalephae – Aphis fabae on Isfahan-Flavarjan, 05-xi-2010”: 1♂; “Lysiphlebus fabarum Phaseolus vulgaris, Isfahan-Najvan, 10-x-2010”: 1♂ and – Nearctaphis bakeri on Trifolium campestre, Isfahan- 1♀; “Lysiphlebus fabarum – Aphis craccivora on Medicago Hoye, 15-v-2011”: 1♂ and 4♀; “Diaeretiella rapae – sativa, Isfahan-Najvan, 25-iv-2011”: 5♂ and 2♀; “Praon Lipaphis pseudobrassicae on Brassica napus, Isfahan- barbatum, Aphidius smithi – Acyrtosiphon pisum on Goldasht, 14-iv-2011”: 2♂ and 1♀; “Diaeretiella rapae, Medicago sativa, Isfahan-Hoye, 27-vii-2010: 1♂ and 2♀; Binodoxys acalephae – Aphis fabae on Phaseolus vulgaris, “Lysiphlebus fabarum – Aphis fabae on Phaseolus vulgaris, Isfahan-Flavarjan, 05-xi-2010”: 5♂ and 3♀; “Lipaphis Isfahan-Filour, 03-ix-2010”: 4♂ and 3♀; “Lysiphlebus pseudobrassicae on Capsella bursa-pastoris, Isfahan- fabarum – Aphis origani on Mentha longifolia, Isfahan- Dourche, 15-iv-2011”: 1♀; “Lysiphlebus fabarum – Aphis Najafabad, 27-iv-2011”: 2♀, Leg. E. Nader. affinis on Mentha longifolia, Isfahan-Dourche, 15-iv- Distribution. Cosmopolitan (Ferrer-Suay et al., 2012a). 2011”: 3♂ and 4♀; “Aphidius matricariae, Praon abjectum Host. HP: Sonchus sp., HA: Aphis sp., HW: unknown; – Aphis solanella on Solanum melongena, Isfahan-Hoye, HP: Sinapis sp., HA: Aphis sp., HW: unknown; HP: 15-x-2010”: 4♂and 1♀; “Adialytus veronicaecola – Aphis Aegopodium sp., Alisma sp., and Platanus sp., HA: Aphis sp., gossypii on Cucurbita pepo, Isfahan-Ghahderijan, 05- HW: unknown (De Gaulle, 1908: 26). HP: unknown, HA: xi-2010”: 5♂ and 3♀; “Lysiphlebus fabarum – Aphis Aphis ambrosia, HW: unknown (Dalla Torre and Kieffer, craccivora on Robinia pseudoacacia, Isfahan-Najvan, 25- 1910: 289). HP: Sinapis alba, HA: Aphis sp., HW: unknown iv-2011”: 2♀; “Lysiphlebus fabarum – Aphis craccivora on (Dalla Torre and Kieffer, 1910: 269). HP: Sonchus asper, HA: Sophora mollis, Isfahan-Dourche, 15-iv-2011”: 7♂ and Aphis sp., HW: unknown (Dalla Torre and Kieffer, 1910: 6♀; “Lysiphlebus fabarum, Aphidius matricariae – Aphis 268). HP: Platanus sp., Alisma plantago, and Aegopodium craccivora on Medicago sativa, Isfahan-Dourche, 15-iv- podagraria, HA: Aphis sp., HW: unknown (Dalla Torre 2011”: 11♂ and 12♀; “Aphidius matricariae, Diaeretiella and Kieffer, 1910: 278). HP:Aulacorthum pelargonii, HA: rapae – Myzus persicae on Brassica napus, Isfahan-Hoye, Myzus ornatus and Rhopalodiphoum padi, HW: unknown 15-x-2010”: 5♂and 7♀; “Lysiphlebus fabarum – Aphis (Valentine, 1975: 60). HP: Quercus sp., HA: Tuberculoides fabae on Beta vulgaris, Isfahan-Flavarjan, 05-xi-2010”: annulatus, HW: Trioxys pallidus; HP: Berberis sp., HA: 2♀; “Aphidius transcaspicus – Hyalopterus pruni on Liosomaphis berberidis, HW: Aphidius hortensis (Vasileva- Phragmites australis, Isfahan-Mobarakeh, 13-xi-2010”: Sumnalieva, 1975: 24). In the Netherlands, the following 2♀; “Praon volucre, Aphidius matricariae, Lysiphlebus combinations were established by Evenhuis: HP: Quercus fabarum, Diaeretiella rapae – Schizaphis graminum on robur, HA: Tuberculoides annulatus, HW: Praon flavinode; Hordeum vulgare, Isfahan-Goldasht, 14-ix-2011”: 3♂ HP: Acer campestre, HA: Periphyllus sp., HW: Trioxys and 1♀; “Aphidius sp. and Lysiphlebus fabarum on Viola falcatus Mackauer; HP: Tilia sp., HA: Eucallipterus tiliae, tricola, Isfahan-Najafabad, 06-vi-2011”: 2♀; “Adialytus HW: an unidentified species of Aphelinidae; HP:Malus veronicaecola, Binodoxys sp. – Aphis rubiae on Rubia sylvestris, HA: Rhopalosiphum insertum, HW: Monoctonus tinctorum, Isfahan-Mobarakeh, 3-xi-2010”: 27♂ and cerasi; HP: Prunus sp., HA: unknown, HW: unknown; HP: 54♀; “Aphidius transcaspicus – Hyalopterus pruni on Phragmites australis, HA: Hyalopterus pruni, HW: Praon Phragmites australis, Isfahan-Mobarakeh, 03-xi-2011”: volucre; HP: Cirsium arvense, HA: Aphis sp., HW: Lysiphlebus 3♂ and 2♀; “Lysiphlebus fabarum – Aphis craccivora on sp; HP: Malus sylvestris, HA: Dysaphis plantaginea, HW: Robinia pseudoacacia, Isfahan-Dourche, 15-iv-2011”: 1♂ Ephedrus persicae; HP: Sinapis arvensis, HA: Brevicoryne and 1♀; “Aphidius matricariae, Lysiphlebus fabarum – brassicae, HW: Diaeretiella rapae; HP: Berberis vulgaris, Aphis craccivora on Trifolium campestre, Isfahan-Isfahan”: HA: Liosomaphis berberidis, HW: Trioxys hortorum; HP: 2♀; “Adialytus salicaphis – Chaitophorus sp. on Populus Sonchus asper and Sonchus oleraceus, HA: Hyperomyzus alba, Isfahan-Mobarakeh, 13-xi-2010”: 19♂ and 21♀; lactucae, HW: Aphidius sonchi Marshall; HP: Galeopsis

1127 FERRER-SUAY et al. / Turk J Zool tetrahit, HA: Cryptomyzus galeopsidis, HW: Aphidius ribis; maritimus, HA: Myzus persicae, HW: unknown; HP: HP: Rosa sp., HA: Macrosiphum rosae, HW: Aphidius Sonchus tenerrimus, HA: unknown, HW: unknown (Suay et rosae; HP: Campanula sp., HA: Uroleucon campanulae, al., 1998: 106). HP: unknown, HA: Capitophorus carduinis HW: Binodoxys centaureae; HP: Urtica dioica, HA: (sic), HW: unknown; HP: unknown, HA: Sitobion sp., HW: Microlophium urticae, HW: Aphidius ervi; HP: Poaceae, HA: Aphidius sp., Ephedrus sp., and Aphelinus sp. (Müller et al., Metopolophium dirhodum, HW: Aphidius uzbekistanicus. 1999: 352). HP: Salix caprea, HA: Aphis farinosa Gmelin, In France, the combinations established by Barbotin and HW: Lysiphlebus confusus (Hübner et al., 2002: 509). HP: identified by Dr. G. Remaudière are: HP: Poa annua, HA: Acer pseudoplatanus, HA: Drepanosiphum platanoides, Rhopalosiphum padi, HW: Ephedrus plagiator, Trioxys HW: Trioxys cirsii; HP: Rapistrum rugosum, HA: Lipaphis auctus, and Aphidius sp.; HP: Mahonia aquifolium, HA: pseudobrassicae, HW: Diaeretiella rapae; HP: Quercus Liosomaphis berberidis, HW: Aphelinus sp.; HP: Leontodon canariensis, HA: Myzocallis castanicola, HW: Trioxys sp., HA: Nasonovia ribisnigri, HW: Aphidius hieraciorum tenuicaudus; HP: Triticum aestivum, HA: Rhopalosiphum Starý; HP: Hordeum murinum, HA: Sitobion avenae, HW: padi, HW: Aphidius colemani (Carver, 2004: 2). HP: Aphidius sp.; HP: Statice sp., HA: Staticobium sp., HW: Solidago altissima, HA: Uroleucon nigrotuberculatum, HW: Praon sp.; HP: Cyperaceae, HA: Rhopalosiphum insertum, Ephedrus plagiator (Takada and Nakamura, 2010: 270). HW: unknown; HP: Lapsana communis, HA: Myzus HP: unknown, HA: Acyrthosiphon pisum, HW: unknown; ornatus, HW: unknown; HP: Gomphocarpus fruticosus, HP: Nothofagus sp., HA: unknown, HW: unknown; HP: HA: Aphis nerii, HW: unknown (Evenhuis and Barbotin, kiwifruit orchard, HA: unknown, HW: unknown (Ferrer- 1977: 185). HP: Artemisia douglasiana, HA: Uroleucon Suay et al., 2012b: 238). HP: Lilium sp., HA: Macrosiphum ambrosiae, HW: Lysiphlebus testaceipes (Andrews, 1978: euphorbiae, HW: unknown; HP: Bromus sp., HA: 32). HP: unknown, HA: Myzus persicae, HW: Diaeretiella Rhopalosiphum padi, HW: Lysiphlebus testaceipes; HP: rapae and Aphidius sp. (Hor, 1984: 19). HP: unknown, Bromus sp., HA: Metopolophium dirhodum, HW: unknown; HA: Therioaphis trifolii, HW: Trioxys complanatus Quilis HP: Bromus sp., HA: Sitobion avenae, HW: unknown; HP: (Wilson and Swincer, 1984: 47). HP: unknown, HA: Aphis Bromus sp., HA: Rhopalosiphum padi, HW: unknown; HP: fabae, HW: Ephedrus persicae, Binodoxys angelicae, and Canna sp., HA: unknown, HW: Aphidius sp.; HP: Alfalfa, Lysiphlebus confusus (Al-Jassani and Al-Adil, 1986: 59). HA: unknown, HW: Lysiphlebus testaceipes (Ferrer-Suay et HP: unknown, HA: Acyrthosiphon kondoi, HW: Aphidius al., 2013a: 40). ervi and Ephedrus plagiator; HP: unknown, HA: Aphis Host remarks. For the following trophic relationships, craccivora, HW: Aphidius colemani; HP: unknown, HA: HP: Berberis vulgaris, HA: Liosomaphis berberidis, HW: Aphis gossypii, HW: Aphidius colemani; HP: unknown, HA: Trioxys hortorum (Evenhuis and Barbotin, 1977), the Aphis nerii, HW: Aphidius colemani; HP: unknown, HA: parasitoid species is most probably Aphidius hortensis, Aphis spiraecola, HW: Aphidius colemani; HP: unknown, which has been incorrectly written as Trioxys hortorum. HA: Brachycaudus helichrysi, HW: Aphidius colemani; Comments. Phaenoglyphis villosa is here recorded for HP: unknown, HA: Brachycaudus persicae, HW: Aphidius the first time in the following associations: Lysiphlebus colemani; HP: unknown, HA: Cavariella aegopodii, HW: fabarum – Aphis affinis, Aphis craccivora, and Nearctaphis Aphidius salicis; HP: unknown, HA: Hyadaphis foeniculi, bakeri; Binodoxys acalephae – Nearctaphis bakeri; Praon HW: Aphidius colemani; HP: unknown, HA: Hyperomyzus abjectum – Aphis solanella; Aphidius transcaspicus – lactucae, HW: Aphidius sonchi; HP: unknown, HA: Myzus Hyalopterus pruni; Adialytus salicaphis – Chaitophorus sp., cerasi, HW: Aphidius colemani; HP: Prunus persicae, HA: Praon yomenae; Aphidius persicus – Uroleucon sonchi; and Myzus persicae, HW: Aphidius colemani; HP: unknown, Praon rosaecola – Macrosiphum rosae. HA: Myzus persicae, HW: Diaeretiella rapae; HP: unknown, HA: Myzus persicae, HW: Ephedrus persicae; HP: unknown, 4. Discussion HA: Rhopalosiphum maidis, HW: Aphidius colemani; The early evidence about Charipinae from Iran included HP: unknown, HA: Rhopalosiphum padi, HW: Aphidius only 5 species of Alloxysta and 1 of Phaenoglyphis colemani; HP: unknown, HA: Rhopalosiphum padi, HW: (Rakhshani et al., 2001; Lotfalizadeh, 2002; Lotfalizadeh Aphidius similis; HP: unknown, HA: Therioaphis trifolli, and van Veen, 2004; Rakhshani et al., 2004; Pujade-Villar HW: Trioxys complanatus; HP: unknown, HA: Toxoptera et al., 2007; Khayrandish-Koshkooei et al., 2013). They citricidus, HW: Aphidius colemani (Carver, 1992: 770). were Phaenoglyphis villosa, Alloxysta citripes, Alloxysta HP: unknown, HA: unknown, HW: Aphidius sp., Ephedrus erythrothorax, Alloxysta consobrina, Alloxysta mullensis, sp., Praon sp., and Trioxys sp. (Höller et al., 1993: 15). and Alloxysta victrix. The most recent work by Ferrer-Suay HP: unknown, HA: unknown, HW: Aphidius sp., Praon et al. (2013e) significantly increased knowledge about the sp., and Ephedrus sp. (Bokina, 1997: 435). HP: Rosa sp., Charipinae from Iran. In this work, 15 Charipinae species HA: Macrosiphum rosae, HW: unknown; HP: Asparagus were determined, of which 9 species were cited for the

1128 FERRER-SUAY et al. / Turk J Zool first time from Iran. Many new host records were also On the basis of the studied material from all over established, in this way broadening the knowledge about the world, and also taking into account data from the the Charipinae in this area. Charipinae worldwide catalogue (Ferrer-Suay et al., Alloxysta consobrina was cited in Iran as Alloxysta 2012a), there are some complexes that repeat in different fuscicornis (Hartig 1841), a well-known cosmopolitan Alloxysta species, such as, for example: Ephedrus persicae species. These 2 have been recently synonymized (Ferrer- – Dysaphis plantaginea in A. arcuata and A. brevis; Suay et al., 2013b). Despite our reservation in establishing Lysiphlebus fabarum – Aphis craccivora in A. arcuata, this synonymy, because the name of A. fuscicornis has A. brevis, A. circumscripta, and A. victrix; Lysiphlebus been used frequently in the bibliography, according to the fabarum – Aphis urticata, Aphis fabae in A. consobrina, A. nomenclature rules, the valid name must be A. consobrina. melanogaster, and A. pleuralis; and Praon volucre – Aphis In the present study, 8 species were determined within fabae in A. arcuata, A. brevis, and A. castanea. Alloxysta 91 host associations from different regions including A. circumscripta was found frequently in association with arcuata, A. brevis, A. circumscripta, A. citripes, A. darci, A. Urolecucon aphids, too. Therefore, it seems that there is mullensis, A. pusilla, and P. villosa; among them, Alloxysta slight host selection, but it is more accurate for the primary circumscripta and A. darci are cited for the first time from parasitoids than for the aphids. It is necessary to continue Iran. Additionally, the important contribution of this work collecting data about the trophic associations related with is that for the already known Charipinae species present the Charipinae in order to get a better idea of the possible in Iran, new data about their trophic relationships are also host selection in this subfamily. given here (see the comments in Section 3). For this reason, it is important to continue with the Currently, some studies aiming to analyze the specificity collections and revisions of the Charipinae material from of the Alloxysta species are in progress (Ferrer-Suay et Iran and other poorly known regions in order to improve al., unpublished data). With this study, we are trying to our knowledge about their trophic relationships. In this elucidate possible host selection by the Charipinae based way, we get to know the trophic relationships in which on qualitative data. Until now, A. citripes has been found they are involved, and, with this, be able to predict the only on the genus Trioxys; the host association Alloxysta impact that their presence can have on important crops citripes – Trioxys pallidus – Chromaphis juglandicola on in the region. Juglans regia seems to be very specific of this Alloxysta species. While some host records for this species seem Acknowledgments doubtful (Dysaphis mali; Belizin, 1966), the other host This research was supported by the projects CGL2008- aphids (Eucallipterus tiliae, Tuberculoides annulatus, 00180 of the Science and Innovation Ministry of Spain Pterocallis alni, and Myzocallis coryli) have a strict affinity and the grant AP2009-4833 of the Education Ministry of to Chromaphis juglandicola, so that the primary parasitoid Spain. The participation by E Rakhshani was supported by was Trioxys pallidus. grant No. 89-9198, University of Zabol.

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