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ÎÖÖ ÎÐîéŹƺƿźƸƃìîƱřźƿřƾſŚƴƃƵźƄůƾƬƬưƫřƲ ǀŝƵźĮƴƧƲǀƫƹř  Study of the genus Cardiochiles (: : Cardiochilinae) in Tehran and Alborz provinces, with one new record from Iran

S. Farahani 1, 2&*, A. A. Talebi 2 and E. Rakhshani 3 1. Research Institute of Forests and Rangeland, Tehran, Iran, Email: [email protected], 2. Department of Agricultural Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box: 14115-336, Tehran, Iran, 3. Department of Plant Protection, College of Agriculture, University of Zabol, Iran.

Abstract Occurrence of the genus Cardiochiles Nees, 1819 (Braconidae: Cardiochilinae) was surveyed in the Northern part of Iran. Cardiochiles Nees, 1819 is a small genus with 63 described species worldwide and 27 species being found in the Palaearctic Region. Material for this study was collected using Malaise traps from Alborz and Tehran provinces during 2010. A total three species belonging to the genus Cardiochiles were identified, C. fallax Kokujev, 1895, C. fumatus Telenga, 1949, C. shestakovi Telenga, 1949, of which C. fumatus is newly recorded from Iran. An updated checklist of Iranian Cardiochiles is provided. Key words: Braconidae, Cardiochilinae, Cardiochiles, new record, Iran

Cardiochiles (Hymenoptera: Braconidae: Cardiochilinae) ƵŶǀĪģ ƶºƳƺĭĨºƿƁŹřżºĭŚºŝƵřźºưƷŻźºŞƫřƹƱřźƸţƽŚƷƱŚŤſřŹŵ žƴūƶƘƫŚƐƯ

 ƱřźƿřƽřźŝŶƿŶū  ƾƳŚƄųŹƱŚƀůřƹƾŞƫŚƏźƜƇřƾ ƬƗƾƳŚƷřźƟřźǀưſ . Cardiochiles Nees, 1819 ƽŚƷƱ ŚŤſřŻřżǀƫŚƯƶƬţŻřƵŵŚƠŤſřŚŝÎÐÕÖƩŚſŹŵŚƷƶ ƳƺưƳ Ŷƃ ƶƘƫŚƐƯ Ʊřźƿř ƩŚưƃ Żř ƾƿŚƷƂ ŴŝŹŵ žƴū Cardiochiles Nees, 1819 ĨºǀŤĩŹŚŘƫŚěƶƤƐƴƯŹŵƶƳƺĭÏÔƹŚǀƳŵŹŵƵŶƃƞǀƇƺţƶƳƺĭÓÐŚŝƾĪģƺĩžƴū ŶƃƽŹƹōƖưū ƱřźƸţ ƹ ŻźŞƫř C. shestakovi Telenga, C. fumatus Telenga, 1949 C. fallax Kokujev, 1895 Cardiochiles ƹ  ƪƯŚƃ žƴūŻřƶƳƺĭƶſŶƃŚŝƾ Ư Cardiochiles C. fumatus 1949 Ʊřźºƿř ƽŚƷƶ ƳƺĭƵŶƃŻƹŹƶŝŢƀǀƫĨģŵƺƃƾ ƯƁŹřżĭƱřźƿřŻřŹŚŝƲǀƫƹřƽřźŝ ƶƳƺĭƶĩ ŶƃƾƿŚſŚƴƃ ŢſřƵŶƿŵźĭƶǀƸţ Cardiochiles Cardiochilinae Braconidae ƱřźƿřŶƿŶūƁŹřżĭ   ƽŶǀƬĩƱŚĭĥřƹ

Introduction  The family Braconidae is the second largest family of Hymenoptera (Aguiar et al., 2013) with approximately 19801 valid species (Yu et al., 2012) and more than 40–50000 species estimated to exist in the world (Sharkey & Wahl, 1992). The subfamily Cardiochilinae Ashmead, 1900 is a small cosmopolitan subfamily of Braconidae with 216 described species, and 41 species being found in the Palaearctic region (Yu et al., 2012). This subfamily is recognizable by spiracle position on the first metasomal latero-tergite, occipital carina completely absent, vein SR1 of fore wing weakly sclerotized and decurved, second submarginal cell broad, scutellum with a more or less developed medioposterior depression (van Achterberg, 1993). Members of the subfamily Cardiochilinae are solitary koinobiont larval endoparasitoids on Lepidoptera, principally Pyralidae and Noctuidae feeding in compact sites such as buds (Shaw & Huddleston, 1991) and are considered as potential biocontrol agents for economic pests (Marsh, 1986; Dangerfield & Austin, 1995; Tillman, 1995). The species appear to be most diverse and abundant in temperate grasslands and tropical forests, especially in seasonally dry forests (Chen et al., 2004). Cardiochiles Nees, 1819 is a small genus with 63 described species worldwide and 27 species being found in the Palaearctic Region (Yu et al., 2012). The genus Cardiochiles was taxonomically studied in European part of Russia (Telenga, 1955; Tobias, 1986), Taiwan (Chou, 1995), Spain (Oltra & Falco, 1997), Russian Far East (Belokobilskij, 1998), Turkey (Inanç, 2002), India (Ahmad & Shuja-Uddin, 2004) and China (Chen et al., 2004). Prior to this study, five species of Cardiochiles were reported from Iran (Telenga, 1955; Hedwig, 1957; Shamszadeh, 1998; Fallahzadeh & Saghaei, 2010; Taghizadeh et al., 2013). Cardiochiles tibialis Hedwig, 1957 and C. triplus Shenefelt, 1973 have been reported only from Iran (Hedwig, 1957; Shenefelt, 1973). In this research, occurrence of Cardiochiles species was studied in Tehran and Alborz provinces. An updated checklist of Iranian Cardiochiles is presented.

st 199 1 Iranian International Congress of Entomology, 29–31 August 2015

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Materials and methods  Sampling was performed using Malaise traps. Sampling was carried out from March to November in Alborz and Tehran provinces during 2010. The specimens were extracted from the Malaise traps and sorted weekly. The captured specimens were extracted from the collecting jars, then treated with mixture of 40% xylene / 60% ethanol 96% for two days, then transferred into amyl acetate for two days and finally placed on a piece of absorbing paper for drying (AXA method, van Achterberg, 2009). The dried specimens were then card-mounted and labeled. Photographs were taken using an Olympus™ SZX9 stereomicroscope equipped with BMZ-04-DZTM digital imaging system (Behin Pajouhesh Co., Iran). All specimens are deposited in the collection of the Department of Entomology, Tarbiat Modares University, Tehran.

Results Three species belong to genus Cardiochiles were collected and identified, of which Cardiochiles fumatus Telenga, 1949 is newly recorded for the Iranian fauna.

Cardiochiles fallax Kokujev, 1895 (fig. 1A−B) Material examined: Tehran province: Peykanshahr, National botanical garden of Iran (35°44′19.91″ N, 51° 10′52.49″ E, 1265 m), 08.vi.2010, 1♀; leg. A. Nadimi. Diagnosis characters (female): Clypeus distinctly defined, with two median teeth; two apical segments of maxillary palp subequal; antennae 38-segmented; propodeum coarsely rugose, with rhombic median area and longitudinal carina between rhombic area and anterior margin of propodeum. Coloration: Head black, antennae black; mesonotum, scutellum and prothorax reddish; fore wing darkened apically, with spot near apical basal cell, second sub-marginal cell darkened (fig. 1B); fore leg reddish, except coxae and trochanter, middle and hind legs black. Distribution: Palaearctic region: Armenia, Azerbaijan, Georgia, Iran, Kazakhstan, Romania, Russia, Tajikistan, Turkey, Ukraine (Yu et al., 2012). Distribution in Iran: Fars (Taghizdeh et al., 2013), Tehran (current study). Host: Myrlaea marmorata (Tobias, 1976, 1986), Etiella zinckenella (Taghizadeh et al., 2013).

*Cardiochiles fumatus Telenga, 1949 (fig. 2A−B) Material examined: Alborz province: Karadj (35°46′08.88″ N, 50°56′55.20″ E, 1277 m), 20.vii.2010, 1♀; Tehran province: Shahriar (35°40′08.10″ N, 50°56′56.64″ E, 1168 m), 07.ix.2010, 1♀; leg. M. Khayrandish. Diagnosis characters (female): Clypeus distinctly defined, with two median teeth venterally; antenna 38- segmented; mesonotum and scutellum smooth and shining, with rugose median groove; propodeum distinctly rugose, with quadrate median area. Coloration: Head and mesosoma reddish; metasoma black; antennal flagellum black, scape red; wings darkened in apically, with spot near basal vein, second sub-marginal cell darkened (fig. 2B); fore leg red, hind leg black; Distribution: Palaearctic region: Afghanistan, Azerbaijan, Kazakhstan, Tajikistan, Uzbekistan, Iran (new record) (Yu et al., 2012). Distribution in Iran: Alborz and Tehran (current study). New record from Iran. Host: Unknown.

st 200 1 Iranian International Congress of Entomology, 29–31 August 2015

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Fig. 1. Cardiochiles fallax Kokujev, 1895: A. Habitus, lateral view, B. Fore wing.

Cardiochiles shestakovi Telenga, 1949 (fig. 3A−B) Material examined: Tehran province: Peykanshahr, National botanical garden of Iran (35°44′19.91″ N, 51° 10′52.49″ E, 1265 m), 18.v.2010, 1♀; leg. A. Mohammadi. Diagnosis characters (female): Clypeus poorly defined, without teeth in ventrally; apical segment of maxillary palp much longer than penultimate segment; antennae 33-segmented; mesonotum and scutellum smooth and shining, with punctate median groove; propodeum distinctly rugose, with large rhombic median area, reaching anterior margin of propodeum. Coloration: Body yellowish; antennae brownish; fore wing darkened apically, second sub-marginal cell transparent (fig. 3B); leg yellowish, except coxae, trochanter, apical hind tibia and hind tarsus black. Distribution: Palaearctic region: Iran, Tajikistan, Turkmenistan, Uzbekistan (Yu et al., 2012). Distribution in Iran: Yazd (Shamszadeh, 1998), Tehran (current study). Host: Unknown.

st 201 1 Iranian International Congress of Entomology, 29–31 August 2015

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Fig. 2. Cardiochiles fumatus Telenga, 1949: A. Habitus, lateral view, B. Fore wing.

Fig. 3. Cardiochiles shestakovi Telenga, 1949: A. Habitus, lateral view, B. Fore wing.

st 202 1 Iranian International Congress of Entomology, 29–31 August 2015

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Discussion  The knowledge of biology of the species of the genus Cardiochiles is mostly restricted (Marsh, 1979; Tobias, 1986; Ma et al., 2002). Cardiochiles shestakovi Telenga, 1949 has been reared from Epischidia caesariella Hampson, 1901 (Lepidoptera: Pyralidae) from Yazd province, central Iran (Shamszadeh, 1998). Epischidia caesariella is the most important pests of Haloxylon sp. in rangeland of Iran. The range of parasitism rate for this species was observed to be % 21−43 during 1993−1996 by Shamszadeh (1998). Cardiochiles fallax has recently been reported as a parasitoid of soybean pod borer, Etiella zinckenella (Treitschke) (Lep.: Pyralidae) from Iran (Taghizadeh et al., 2013). Among the neighboring countries of Iran, Telenga (1955) and Tobias & Alexeev (1977) were reported 16 species of Cardiochiles from Turkmenistan. From the eastern neighboring countries, Cardiochiles erythronotus Cameron, 1906 has been recorded from Pakistan (Cameron, 1906 ), and C. pseudofallax Telenga, 1955 and C. fumatus Telenga, 1949 have been reported from Afghanistan (Tobias, 1986; Tobias et al., 1998). Inanç and Beyarslan (1994) and Inanç (2002) listed 4 species of the genus Cardiochiles from Turkey. The results of this study and review of the previously recorded taxa revealed the existence of six species in Iran (Table 1). Up to now, Cardiochiles tibialis and C. triplus have been reported only from Iran. Cardiochiles triplus has already been recorded by Hedwig (1957) from Sistan and Baluchestan province, but under the name of C. minutus Hedwig, 1957 which is a junior synonym (Shenefelt, 1973). Among the Iranian species of Cardiochiles, C. saltator (Fabricius, 1781) was a particularly widespread species (35 countries) and was recorded by Telenga (1955) from Iran as C. brachialis Rondani, 1877, which is considered as a junior synonym of C. saltator (Dangerfield et al., 1999). Species of the genus Cardiochiles are rarely collected group because they are frequently found in semi-arid (sub)tropical areas (van Achterberg, 1993). Because Iran is a large country, incorporating various geographical regions and climates, we expect that the Cardiochiles species of Iran will be substantially increased.

Table 1. Updated list of Cardiochiles species recorded from Iran Distribution in Iran Cardiochiles species References (provinces) Cardiochiles fallax Kokujev, 1895 Fars Taghizadeh et al. (2013) Tehran Current study Cardiochiles fumatus Telenga,1949 Alborz and Tehran Current study Cardiochiles saltator (Fabricius, 1781) Not defined Telenga (1955) Not defined Belokobylskij (1998) Isfahan Ghahari et al. (2011) Cardiochiles shestakovi Telenga, 1949 Yazd Shamszadeh (1998) Tehran Current study Cardiochiles tibialis Hedwig, 1957 Sistan & Baluchestan Hedwig (1957) Cardiochiles triplus Shenefelt, 1973 Sistan & Baluchestan Hedwig (1957) Not defined Shenefelt (1973)

Acknowledgements This study was supported by the Department of Entomology, Tarbiat Modares University, Tehran, which is greatly appreciated. Our special thanks are expressed to Dr. A. Mohammadi, Dr. A. Nadimi and Dr. M. Khayrandish for helping us collect the specimens.

st 203 1 Iranian International Congress of Entomology, 29–31 August 2015

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