J Biodivers Syst 05(3): 159–169 ISSN: 2423-8112

JOURNAL OF INSECT BIODIVERSITY AND SYSTEMATICS

Research Article http://jibs.modares.ac.ir http://zoobank.org/References/D262CA64-B31D-4EEC-BFCE-24B610103957

Faunistic study of the genus Habrobracon Ashmead (: ) from Iran

Mohammad Zargar1, Ali Asghar Talebi1* and Samira Farahani2

1 Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P. O. Box: 14115-336, Tehran, Iran. 2 Research Institute of Forests and Rangelands, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran.

ABSTRACT. Habrobracon kopetdagi Tobias, 1957 and H. ponticus (Tobias, Received: 1986) are collected from Khuzestan province and recorded for the first time 26 May, 2019 from Iran. In addition, three species (viz., H. crassicornis (Thomson, 1892), H.

Accepted: iranicus Fischer, 1972, H. stabilis (Wesmael, 1838)) are new provincial records. 25 June, 2019 A faunistic list of Iranian Habrobracon species with distribution, host records and brief diagnoses for new recorded species from Iran are provided. Published: 01 July, 2019

Subject Editor: Ali Ameri Key words: Khuzestan, new records, faunistic list, Iran

Citation: Zargar, M., Talebi, A.A. & Farahani, S. (2019) Faunistic study of the genus Habrobracon Ashmead (Hymenoptera: Braconidae) from Iran. Journal of Insect Biodiversity and Systematics, 5 (3), 159–169.

Introduction (Hymenoptera: Braconidae) is a differs from in having 1) vein 3-SR large subfamily with about 190 genera and less than l.5 times vein r in Habrobracon vs over 3000 described species worldwide more than 1.9 times in Bracon and 2) vein 2- (Quicke, 2015; Yu et al., 2016). Habrobracon SR+M long in Habrobracon vs short in Ashmead, 1895 is a moderate genus of the Bracon. subfamily Braconinae, with 37 valid species The species of Habrobracon parasitize worldwide (Yu et al., 2016). The status of about 235 species of the order , Habrobracon (as well as most subgenera of mostly Gelechiidae, Noctuidae, the Bracon genus group) is not established and Tortricidae (Yu et al., 2016). Habrobracon adequately. In absence of strong morphological criteria in determining the hebetor Say species complex are the most members of this taxon, different authors well-studied species in this genus, as well considered it as either a separate genus as in the whole subfamily Braconinae and (Quicke, 1987; Papp, 2008, 2012) or a are extensively used as bio-control agent of subgenus of Bracon (Tobias, 1986; van the important stored product pests, such as Achterberg & Polaszek, 1996; Yu et al., Ephestia kuehniella Zeller (Pyralidae), Plodia 2016). In present study we consider interpunctella Hubner (Pyralidae) and Habrobracon to be a valid genus. Habrobracon Angoumois grainmoth (Gelechiidae).

Corresponding authors: Ali Asghar Talebi, E-mail: [email protected] Copyright © 2019, Zargar et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 160 Habrobracon in Khuzestan province

To date, ten species of the genus Habrobracon kopetdagi Tobias, 1957 and H. Habrobracon have been reported from Iran ponticus (Tobias, 1986) are recorded for first (Modarres Awal, 1997; Karampour & time from Iran. The list of species is given Fasihi, 2004; Dezianian & Quicke, 2006; below. Lashkari Bod et al., 2011; Ghahari & Fischer 2011; Ghahari et al., 2011, 2012; Ameri et Family Braconidae Nees, 1811 al., 2014; Farahani et al., 2016; Rajabi Subfamily Braconinae Nees, 1811 Mazhar et al., 2019). Considering the low Genus Habrobracon Ashmead, 1895 number of known Habrobracon species from Iran (10 out of 23 distributed in Habrobracon brevicornis (Wesmael, 1838) Palaearctic), taxonomic and faunistic Original name. Braco brevicornis Wesmael, studies on this subgenus is required. In the 1838 present study, two new distributional Distribution in Iran. Bushehr (Karampour records and a faunistic list along with & Fasihi, 2004), Ilam (Gharali, 2004), distribution and host records are provided. Semnan (Dezianian & Jalali, 2004). Material and methods General distribution. Worldwide The specimens were collected from (introduced into Nearctic) (Yu et al., 2016). Khuzestan province during 2016–2017 Host records. Lepidoptera: Crambidae, using Malaise traps. Khuzestan province Depressariidae, Erebidae, Gelechiidea, includes mountainous areas located in the Lymantriidae, Noctuidae, Nolidae, north with plains and sea level areas in the Plutellidae, Pyralidae, Tineidae, south. The specimens were fortnightly Tortricidae, Xyloryctidae, Yponomeutidae removed from the collecting bottle and (Yu et al., 2016). preserved in 70% alcohol. Later, the Remark. Habrobracon brevicornis, the former specimens were prepared according to the synonym of H. hebetor, has been re- AXA method (van Achterberg, 2009) and validated based on molecular data (Kittel & mounted on triangular cards and Maeto, 2018). eventually labeled. The key by Tobias (1986) and comparison with the type Habrobracon concolorans (Marshall, 1900) material of all the listed species were used Original name. Bracon concolorans Marshall, for identification of the specimens. 1900 Photographs of the specimens were taken under a microscope (OlympusTM AX70) or Synonyms. Bracon (Bracon) concolor stereomicroscope (OlympusTM SZX9) Thomson, 1892, Habrobracon nigricans equipped with digital camera (Sony, Szepligeti, 1901, H. mongolicus Telenga, Japan). The terminology of morphological 1936. characters follows van Achterberg (1988, Distribution in Iran. Fars (Lashkari Bod et 1993). Abbreviations used in this paper are al., 2011, as H. nigricans), Hormozgan as follows: POL = postocellar line, OOL = (Ameri et al., 2014, as Bracon (Habrobracon) ocularocellar line, MOD = median ocellar nigricans), Kerman (Iranmanesh et al., 2018) diameter. General distribution: Palaearctic, Oriental Results (Yu et al., 2016). A total of 12 species of the genus Host records: Coleoptera: Anobiidae, Habrobracon (Braconidae: Braconinae) are Lepidoptera: Gelechiidae, Tortricidae, listed from the Iranian fauna, of which Pyralidae (Yu et al., 2016).

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Habrobracon crassicornis (Thomson, 1894) vernalis Szépligeti, 1901, Habrobracon Original name. Bracon (Bracon) crassicornis beneficientior Viereck, 1911, Habrobracon Thomson, 1892 plotnicovi Bogoljubov, 1914, Bracon breviantennatus de Stefani, 1919, Synonym. Habrobracon (Habrobracon) Habrobracon serinopae Cherian, 1929, flavosignatus Tobias, 1957. Habrobracon tortricidarum Goidanich, 1934, Material examined. Southwestern Iran, Habrobracon pectinophorae Watanabe, 1935, Khuzestan province: Baghmalek, Ghaletol Bracon (Habrobracon) hebetor asiaticus [31°37ʹ49″ N, 49°52′53″ E], 880 m a.s.l., 5– Telenga, 1936, Habrobracon flavus Telenga, 19.II.2017, 1♀, Malaise trap in citrus 1936, Habrobracon turkestanicus Telenga, orchards, leg.: M. Zargar. 1936, Habrobracon lozinskii Bogacev, 1939. Distribution in Iran. Ilam (Ghahari et al., Material examined. Southwestern Iran, 2011), Khuzestan (current study). Khuzestan province: Khoramshahr, Sheneh General distribution. Palaearctic (Yu et al., [30°25ʹ32″ N, 48°11′20″ E], 2 m a.s.l., 8– 2016). 22.VI.2016, 2♀♀; 7–21.III.2017, 4♀♀; 8– 22.VII.2017, 3♀♀; Malaise trap in palm Host records. Lepidoptera: Gelechiidae, orchards, leg.: M. Zargar. Pyralidae, Tortricidae, Yponomeutidae (Yu et al., 2016). Distribution in Iran. East Azarbaijan (Modarres Awal, 1997), Fars (Lashkari Bod Habrobracon didemie (Beyarslan, 2002) et al., 2011), Hormozgan (Ameri et al., Original name. Bracon (Habrobracon) didemie 2014), Isfahan (Bagheri & Nematollahi, Beyarslan, 2002 2006), Kerman, Tehran (Modarres Awal, 1997), Khuzestan (current study), Distribution in Iran. Hormozgan (Ameri Kermanshah (Noori, 1994), Qom (Norouzi et al., 2015) et al., 2009), West Azarbaijan (Modarres General distribution. Palaearctic (Yu et al., Awal, 1997). 2016). General distribution. Worldwide (Yu et Host record. Unknown. al., 2016). Host records. Coleoptera: Chrysomelidae, Habrobracon excisus Tobias, 1957 Curculioniade, Tenebrionidae. Hemiptera: Original name. Habrobracon (Habrobracon) Anthocoridae. Hymenoptera: Braconidae, excisus Tobias, 1957 Ichneumonidae, Ceraphronidae, Chalcididae, Distribution in Iran. Iran (exact location is Cynipidae, Encyrtidae, Eulophidae, not known) (Haeselbarth, 1983; Fallahzadeh Eurytomidae, Pteromalidae. Lepidoptera: & Saghaei, 2010). Arctiidae, Depressariidae, Gelechiidae, General distribution: Palaearctic (Yu et al., Lymantriidae, Noctuidae, Nolidae, 2016). Papilionidae, Pieridae, Plutellidae, Pyralidae, Saturniidae, Tortricidae, Host records. Lepidoptera: Depressariidae Yponomeutidae (Yu et al., 2016). (Yu et al., 2016). Habrobracon iranicus Fischer, 1972 Say, 1836 Original name. Habrobracon iranicus Fischer, Original name. Bracon hebetor Say, 1836 1972 Synonyms. Bracon dorsator Say, 1836, Bracon Material examined. Southwestern Iran, juglandis Ashmead, 1889, Habrobracon Khuzestan province: Behbahan, Dodangeh brunneus Szépligeti, 1901, Habrobracon [30°42ʹ08″ N, 50°10′41″ E], 300 m a.s.l., 8-

162 Habrobracon in Khuzestan province

22.VII.2017, 1♀; Malaise trap in citrus long as its apical width, coriaceous, second orchards, leg.: M. Zargar. metasomal tergite more sculptured Distribution in Iran. Tehran (Modarres compared to next tergites (Fig. 1E). Awal, 1997), Khuzestan (current study), Coloration: Body mostly black, inner side Iran (exact location is not known) (Fischer, of eyes with reddish pattern, mandibles 1972; Shenefelt, 1978). yellowish (Fig. 1F). General Distribution. Western Palaearctic Habrobracon ponticus (Tobias, 1986) (Yu et al., 2016). Original name. Bracon (Habrobracon) Host records. Lepidoptera: Noctuidae, ponticus Tobias, 1986 Tortricidae, Yponomeutidae (Modarres Material examined. Southwestern Iran, Awal, 1997). Khuzestan province: Lali, Taraz [32°20ʹ 49″ Habrobracon kopetdagi Tobias, 1957 N, 49°05′11″ E], 390 m a.s.l., 21.III– 4.IV.2017, 1♀; Malaise trap in citrus (Fig. 1) orchards, leg.: M. Zargar. Original name. Habrobracon (Habrobracon) Distribution in Iran. Khuzestan (current kopetdagi Tobias, 1957 study). New record for Iran. Material examined. Southwestern Iran, General Distribution. Palaearctic (Yu et Khuzestan province: Ramhormoz, al., 2016). Gharabad [30°59ʹ37″ N, 49°46′50″ E], 126 m a.s.l., 22.V-5.VI.2017, 2♂♂; Malaise trap in Host record. Unknown. olive orchards, leg.: M. Zargar. Diagnosis: Head width 2.0 times its length Distribution in Iran. Khuzestan (current in dorsal view; POL: MOD:OOL = 3:2:6 study). New record for Iran. (Fig. 2A); malar space 1.2 times basal width of mandible; width of face 1.8 times General distribution. Palaearctic (Yu et al., its height (Fig. 2B); antenna 22-segmented, 2016). shorter than body, length of penultimate Host records. Coleoptera: Buprestidae. segment 1.5 times its width; length of Lepidoptera: Gelechiidae (Yu et al., 2016). mesosoma 1.7 times its maximum height; Diagnosis (male): Head width 1.9 times its mesoscutum granulose (Fig. 2C); length in dorsal view; POL:MOD:OOL = propodeum granulose, without median 3:2:6 (Fig. 1A); malar space subequal to carina; marginal cell in fore wing ending basal width of mandible; width of face 1.7 clearly before tip of wing, vein 1-R1 as long times its height (Fig. 1B); antenna 27- as pterostigma, vein 3-SR 1.3 as long as segmented, longer than body, length of vein r, 0.75 times as long as vein 2-SR; penultimate segment 1.7 times its width; pterostigma 3 times as longer than width length of mesosoma 1.2 times its maximum (Fig. 2D); length of first metasomal tergite height; mesoscutum granulose (Fig. 1C), 0.75 times as long as its apical width, with two smooth longitudinal stripes in granoluse (Fig. 2E). Coloration: Body middle part; propodeum granulose, mostly black, lower side of abdomen with without median carina; fore wing vein 1-R1 reddish or dark brownish yellow pattern, as long as pterostigma, vein 3-SR 1.3 times mandibles yellowish red, anterior margin as long as vein r, 0.9 times as long as vein of clypeus and hind tibiae in basal half 2-SR; pterostigma 2.8 times longer than reddish dark brown, wings darkened (Fig. wide (Fig. 1D); first metasomal tergite as 2F).

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Figure 1. Habrobracon kopetdagi (Tobias, 1957), A. Head, dorsal view; B. Head, frontal view; C. Mesosoma, dorsal view; D. Fore wing; E. Metasoma, dorsal view; F. Habitus, lateral view.

164 Habrobracon in Khuzestan province

Figure 2. Habrobracon ponticus Tobias, 1986, A. Head, dorsal view; B. Head, frontal view; C. Mesosoma, dorsal view; D. Fore wing; E. Metasoma, dorsal view; F. Habitus, lateral view.

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Habrobracon radialis Telenga, 1936 Discussion Original name. Habrobracon radialis This survey, for the first time, was carried Telenga, 1936 out in Khuzestan province in the Distribution in Iran. Golestan (Sakenin et southwestern part of Iran. Geographically, al., 2012), Guilan (Ghahari et al., 2012), this province is covered by mountainous Semnan (Dezianian & Quicke, 2006). areas in the north and the plains and sea level regions in the south. The sampling General Distribution. Palaearctic (Yu et al. sites, for this study, include both zones. 2016). Because of the specific geographic Host records. Lepidoptera: Gelchiidae, conditions, the flora of Khuzestan is Plutellidae (Yu et al., 2016). varying from mountainous trees in highlands to marshlands in low elevation Habrobracon stabilis (Wesmael, 1838) areas (Hoberlandt, 1983). Original name. Braco stabilis Wesmael, 1838 The result of this study led to Synonym. Bracon opacus Stelfox, 1953 identifying six species of genus Habrobracon Material examined. Southwestern Iran, Ashmead, 1895, which increased the total Khuzestan province: Ramhormoz, number of Iranian Habrobracon to twelve. Gharabad [30°59ʹ37″ N, 49°46′50″ E], 126 m Moreover, three species are recorded, for a.s.l., 5–19.II.2017, 1♀; 7–21.III.2017, 1♀; the first time, from Khuzestan province. Malaise trap in olive orchards, leg.: M. According to the previous literature on Zargar. the genus Habrobracon in the different parts Distribution in Iran. Hamadan (Rajabi of Iran, the H. hebetor Say, 1836 species Mazhar et al., 2019), Khuzestan (current complex has the most dispersal in Iran with study), Qazvin province (Ghahari & seven provincial records (Fig. 3) (Modarres Fisher., 2011). Awal, 1997; Karampour & Fasihi, 2004; Dezianian & Quicke, 2006; Lashkari Bod et General Distribution. Nearctic, Orienal, al., 2011; Ameri et al., 2014; Farahani et al., Palaearctic (Yu et al., 2016). 2016). It should be noted that the provinces Host records. Coleoptera: Dermestidae, located in south (Hormozgan with four Anobiidae, Curculionidae. Diptera: recorded species) (Ameri et al., 2014) and . Lepidoptera: Coleophoridae, southwest (Khuzestan with 6 recorded Depressariidae, Gelechiidae, Tortricidae, species) (Modarres Awal, 1997; current Yponomeutidae (Yu et al., 2016). study) are more species rich than other provinces of Iran (Fig. 3). Habrobracon telengai Muljarskaya, 1955 Considerable studies have been Original name. Habrobracon telengai performed on the genus Habrobracon in the Mulyarskaya, 1955 Palaearctic region including about 23 species Distribution in Iran. Hormozgan (Ameri known from the countries adjacent to Iran et al., 2014), Kerman (Mehrnejad, 2010). (Yu et al., 2016). Considering the number of General Distribution. Palaearctic (Yu et Habrobracon species revealed in Khuzestan al., 2016). province and the potential role of its species in biological control, further integrated Host records. Coleoptera: Buprestidae, taxonomic and faunistic research along with Curculionidae. Lepidoptera: Gelechiidae, revealing the host associations are essentially Tortricidae (Yu et al., 2016). required.

166 Habrobracon in Khuzestan province

Figure 3. Provincial distribution species of subgenus Habrobracon Ashmead, 1895.

Acknowledgments Conflict of Interests Thanks are due to the Department of The authors declare that there is no conflict Entomology, Tarbiat Modares University of interest regarding the publication of this for providing financial support for this paper. study. We are most grateful to Dr. References Konstantin Samartsev (Zoological Institute Ameri, A., Talebi, A.A., Beyarslan, A., Kamali, K. of the Russian Academy of Sciences) for & Rakhshani, E. (2014) Study of the genus valuable help in identification of the Bracon Fabricius, 1804 (Hymenoptera: Braconidae) of Southern Iran with description species and very helpful comments on the of a new species. Zootaxa, 3754, 353‒380. earlier version of the manuscript. http://dx.doi.org/10.11646/zootaxa.3754.4.2

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مطالعة فونستیک جنس Hymenoptera: Braconidae) Habrobracon Ashmead) در ایران

محمد زرگر1، علی اصغر طالبی1* و سمیرا فراهانی2

1 گروه حشره شناسی، دانشکده کشاورزی، دانشگاه تربیت مدرس، صندوق پستی 333-11111 ،تهران، ایران. 2 مؤسسه تحقیقات جنگلها و مراتع، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران. * پست الکترونیکی نویسنده مسئول مکـاتبه: [email protected] تاریخ دریـافت: 50 خرداد 1389 ، تاریخ پذیرش: 50 تیر 1389 ، تاریخ انتشار: 15 تیر 1389

چکیـده: دو گونه (Habrobracon kopetdagi (Tobias, 1957 و H. ponticus Tobias, 1986 از استان خوزستان جمع آوری گردید و برای اولین بار از ایران گزارش میشوند. عالوه بر این سه گونه H. iranicus ، H. crassicornis Thomson, 1892 (H. stabilis (Wesmael, 1838) ،(Fisher, 1972 برای اولین بار از استان خوزستان گزارش میشوند. لیست گونههای جنس Habrobracon به همراه پراکنش، میزبانها و خصوصیات تفکیکی برای گزارشهای جدید از ایران ارایه شد.

واژگـان کلیدي: خوزستان، گزارش، لیست گونهها، میزبان