Egypt. J. Plant Prot. Res. Inst. (2020), 3 (1): 398 - 408

Egyptian Journal of Plant Protection Research Institute

www.ejppri.eg.net

A faunistic study on (: Apoidea) of Northern Iran

Hamid, Sakenin1; Shaaban, Abd-Rabou2; Nil, Bagriacik3; Majid, Navaeian4; Hassan, Ghahari4 and Siavash, Tirgari5 1Department of Plant Protection, Qaemshahr Branch, Islamic Azad University, Mazandaran, Iran. 2Plant Protection Research Institute, Agricultural Reseach Center, Dokki, Giza, Egypt. 3 Niğde Omer Halisdemir University, Faculty of Science and Art, Department of Biology, 51100 Niğde Turkey. 4Faculty of Engineering, Yadegar- e- Imam Khomeini (RAH) Shahre Rey Branch, Islamic Azad University, Tehran, Iran. 5Department of Entomology, Science and Research Branch, Islamic Azad University, Tehran, Iran. ARTICLE INFO Abstract: Article History In this faunistic research, totally 24 species of Received: 11/ 2/ 2020 Megachilidae (Hymenoptera) from 8 genera Accepted: 20/ 3 /2020 Fabricius, 1805, Chelostoma Latreille, 1809, Coelioxys Keywords Latreille, 1809, Haetosmia Popov, 1952, Hoplitis Klug, 1807, Megachilidae, Apocrita, Lithurgus Berthold, 1827, Megachile Latreille, 1802, Osmia fauna, distribution and Panzer, 1806 were collected and identified from different Iran. regions of Iran. Two species are new records for the fauna of Iran: Coelioxys (Coelioxys) aurolimbata Förster, 1853, and Megachile (Eutricharaea) apicalis Spinola, 1808.

Introduction Megachilidae (Hymenoptera) with belonging to the Megachilidae are more than 4000 described species effective pollinators in some plants worldwide (Michener, 2007) is a large (Bosch and Blas, 1994 and Vicens and family of specialized, morphologically Bosch, 2000). These solitary are rather uniform bees found in a wide both ecologically and economically diversity of habitats on all continents relevant; they include many pollinators of except Antarctica, ranging from lowland natural, urban and agricultural vegetation tropical rain forests to deserts to alpine (Gonzalez et al., 2012). Furthermore, it environments (Litman et al., 2011). The has been reported that the Megachilidae front wings without exception have got species can be used as a commercial two marginal cells, and the stigma is species when a decrease is observed in small. The pollen-collecting scopa of all the primary pollinator belonging to the nonparasitica females is located on the other family (Richards, 1997 and Güler abdominal sterna (Stephen et al., 1969 and Çağatay, 2006). and Özbek and van der Zanden, 1992). It The fauna of Iranian has been reported that some species Megachilidae has been studied rather

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Sakenin et al., 2020 well and several papers were published tribes, and valid species names are listed by Popov (1967), Esmaili and Rastegar alphabetically within genera, together (1974), Warncke (1981), Ebadi (1995), with general distribution. Talebi et al. (1995), Modarres Awal Family Megachilidae Latreille, 1802 (1997), Izadi et al. (1998, 1999, 2000, Subfamily Megachilinae Latreille, 1802 2004, and 2006), Karimpour et al. Tribe Anthidiini Ashmead, 1899 (2002), Engel (2006), Tavakkoli et al. Genus Anthidium Fabricius, 1805 (2010), Khaghaninia et al. (2010), 1. Anthidium (Anthidium) florentinum Khodaparast et al. (2011), Monfared and (Fabricius, 1775) Khodaparast (2012), Rasekh Adel et al. Material examined: Golestan province, (2012 a, b and c), Salehi Sarbijan et al. Minudasht, 37°10′N 55°30′E, 2♀♀, 1♂, (2012), Soraya Mohtat et al. (2012), October 2012; Mazandaran province, Keshtkar et al. (2012 and 2015), Sari, 36°30′N 53°30′E, 1♀, June 2013. Khodaparast and Monfared (2012 and General distribution: Asia Minor, 2013), Monfared et al. (2012) and Caucasus, Central Asian part of the Nadimi et al. (2013a, b and 2014). former USSR, South and Central Europe, The aim of this research is a Siberia, Syria (Banaszak and partial faunistic survey on Megachilidae Romasenko, 1998), Iran (Warncke , of Golestan and Mazandaran provinces 1980) and USA (Comba and Comba (North of Iran). 1991). Material and methods Plant association: Polylectic (Fabaceae The specimens of this research and Lamiaceae) (Banaszak and were collected by sweeping net and Romasenko, 1998), Medicago sativa Malaise traps from some regions of (Fabaceae), Euphorbia (Euphorbiaceae) northern Iran (Golestan and Mazandaran and Epilobium hirsutum (Onagraceae) provinces). The collected specimens were (Khodaparast and Monfared, 2012). placed in ordinary paper envelopes after Comments: This species was collected being killed with cyanid, and then placed from and onion fields, and is a in a desiccator to prepare them for dominant species in alfalfa fields morphological study. The materials were (Rasekh Adel et al., 2012 b and c). pinned and labeled according to current Tribe Lithurgini Newman, 1834 taxonomic rules and were examined with Genus Lithurgus Berthold, 1827 a stereomicroscope. For the 2. Lithurgus cornutus (Fabricius, 1787) determination of the genera and species, Material examined: Golestan province, the keys developed by Osychnyuk et al. Kalaleh, 37°43′N 55°49′E, 2♀♀, July (1978), Dorn and Weber (1988), 2012. Warncke (1980 and 1992), Banaszak and General distribution: Iran (Warncke Romasenko (1998), Scheuchl (2006), 1981), Asia Minor, Caucasus, Michener (2007) and Amiet et al. (2004) Kazakhstan, North Africa, South, East were used. Classification of the different and Central Europe (Banaszak and taxa follows Michener (2007). Romasenko, 1998), China, Greece, Results and discussion Hungary, Italy, Japan, Morocco, In this research, 24 species of Romania, Taivan, Turkey, the former Megachilidae are recorded from Golestan USSR, and former Yugoslavia (van den and Mazandaran provinces (North of Zanden, 1986). Iran). Names of the valid genera within

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Plant association: Oligolectic General distribution: North, South and (Asteraceae) (Banaszak and Central Europe (Banaszak and Romasenko, 1998 and Güler and Romasenko, 1998). Sorkun, 2007). Plant association: Polylectic (Rosaceae, Tribe Megachilini Latreille, 1802 Fabaceae and Caprifoliaceae) (Banaszak Genus Coelioxys Latreille, 1809 and Romasenko, 1998). 3. Coelioxys (Coelioxys) aurolimbata 7. Megachile (Megachile) pilicrus Förster, 1853 Morawitz, 1878 Material examined: Mazandaran Material examined: Golestan province, province, Savadkooh, 36°05′N 52°55′E, Kordkoy, 36°41′N 54°12′E, 2♀♀, August 1♂, August 2014. 2009. General distribution: Caucasus, Central General distribution: Caucasus, Central Asian part of the former USSR, Europe, Asian part of the former USSR North Africa and Turkey (Banaszak and (Banaszak and Romasenko, 1998), Romasenko, 1998). South, Eastern and Central Europe Comments: New record for Iran. (Comba and Comba, 1991). Genus Megachile Latreille, 1802 8. Megachile (Eutricharaea) rotundata 4. Megachile (Eutricharaea) apicalis (Fabricius, 1787) Spinola, 1808 Material examined: Mazandaran Material examined: Mazandaran province, Savadkooh, 36°05′N 52°55′E, province, Behshahr, 36°41′N 53°44′E, 4♀♀, 3♂♂, August 2014; Golestan 2♀♀, 1♂, June 2013. province, Minudasht, 37°10′N 55°30′E, General distribution: Canada, 1♀, 1♂, October 2012. Caucasus, Central Asian part of the General distribution: Caucasus, Central former USSR, North Afiica, South and Asian part of the former USSR, Europe, Central Europe (Banaszak and Far East Russia, Kazakhstan, North Romasenko, 1998). Africa, North and South America, New Comments: New record for Iran. Zeland (Comba and Comba, 1991 and 5. Megachile (Eutricharaea) leachella Banaszak and Romasenko, 1998), Curtis, 1828 Turkey (Özbek and van der Zanden, Material examined: Mazandaran 1994). province, Ramsar, 36°47′N 50°32′E, 1♂, Plant association: Polylectic September 2012. (Asteraceae, Fabaceae and Lamiaceae) General distribution: Asia, Caucasus, (Banaszak and Romasenko, 1998). Europe, North Africa, North America, Tribe Osmiini Newman, 1834 Russain Far East, Siberia (Banaszak and Genus Chelostoma Latreille, 1809 Romasenko, 1998) and Iran 9. Chelostoma (Chelostoma) (Khaghaninia et al., 2010). emarginatum (Nylander, 1856) Plant association: Polylectic (mainly Material examined: Mazandaran Fabaceae) (Banaszak and Romasenko, province, Behshahr, 36°41′N 53°44′E, 1998). 1♀, 1♂, June 2013. 6. Megachile (Xanthosarus) nigriventris General distribution: Austria, Schenck, 1870 Azerbaijan, Bulgaria, Bosnia- Material examined: Golestan province, Herzegovina, Croatia, Czech Republic, Kordkoy, 36°41′N 54°12′E, 1♀, 2♂♂, France, Greece, Hungary, Iran, Italy, September 2009. Macedonia, Portugal, Romania, Serbia

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Sakenin et al., 2020 and Montenegro, Sicily, Slovakia, 13. Hoplitis (Hoplitis) flabellifera Slovenia, Spain, Switzerland, Turkey (Morice, 1901) (Grace, 2010 and Müller, 2012). Material examined: Mazandaran Plant association: Oligolectic on province, Amol, 36°28′N 52°21′E, 3♀♀, Ranunculus (Ranunculaceae) and 1♂, April 2013. possibly also on closely related genera General distribution: Armenia, Iran, (Amiet et al., 2004; Sedivy et al., 2008; Jordan, Palestine, Syria, Turkey (Grace, Grace 2010 and Müller 2012). 2010 and Müller, 2012). 10. Chelostoma (Gyrodromella) Plant association: Polylectic with a proximum Schletterer, 1889 strong preference for Anchusa Material examined: Golestan province, (Boraginaceae) (Müller, 2012), Vicia Kalaleh, 37°43′N 55°49′E, 2♀♀, (Fabaceae), Borago officinalis September 2012. (Boraginaceae), Centuria (Asteraceae) General distribution: Azerbaijan, (Khodaparast and Monfared, 2012), Caucasus, China, Far East, Georgia, Iran, Vicia (Asteraceae), Borago officinalis Russia, Turkmenistan, Turkey, Ukraine (Boraginaceae), Centaurea (Asteraceae) (Banaszak and Romasenko 1998 and (Khodaparast and Monfared, 2013). Grace, 2010). Genus Osmia Panzer, 1806 Plant association: Probably Oligolectic 14. Osmia (Monosmia) apicata Smith, on Campanulaceae (Banaszak and 1853 Romasenko, 1998 and Müller, 2012). Material examined: Mazandaran Genus Haetosmia Popov, 1952 province, Behshahr, 36°41′N 53°44′E, 11. Haetosmia vechti (Peters, 1974) 2♀♀, June 2013. Material examined: Mazandaran General distribution: Albania, Armenia, province, Savadkooh, 36°05′N 52°55′E, Bulgaria, Croatia, Iran, Italy, Jordan, 1♀, 2♂♂, August 2014. Georgia, Greece, Macedonia, Palestine, General distribution: Greece, Iran, Russia, Serbia and Montenegro, Slovenia, Palestine, Turkey (Banaszak and Syria, Turkey (Grace, 2010 and Müller, Romasenko 1998; Grace 2010 and 2012). Müller, 2012). Plant association: Oligolectic on Plant association: Oligolectic on Onosma sp. (Boraginaceae) (Müller, Heliotropium (Boraginaceae) 2012). (Mavromoustakis, 1954). 15. Osmia (Osmia) bicornis (Linnaeus, Genus Hoplitis Klug, 1807 1758) 12. Hoplitis (Hoplitis) adunca (Panzer, Material examined: Mazandaran 1798) province, Qaemshahr, 36°28′N 52°52′E, Material examined: Golestan province, 2♀♀, 2♂♂, August 2014. Gorgan, 36°50′N 54°30′E, 1♀, spring General distribution: Algeria, Cyprus, 2012. Europe, Far Eastern Siberia, Iran, General distribution: Asia Minor, Kazakhstan, Kyrgyzstan, Morocco, Caucasus, Central Asian part of the Tunisia, Turkmenistan, Palestine, Syria, former USSR, North Africa (Warncke Turkey (Banaszak and Romasenko, 1992; Banaszak and Romasenko, 1998 1998; Grace, 2010 and Müller 2012). and Amiet et al., 2004), South, Eastem Plant association: Polylectic, prefer and Central Europe (Comba and Rosaceae and Fabaceae (Banaszak and Comba, 1991). Romasenko, 1998 and Müller, 2012).

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16. Osmia (Metallinella) brevicornis Europe, Syria, Tunisia, Turkey and (Fabricius, 1798) Turkmenistan (Banaszak and Material examined: Golestan province, Romasenko, 1998; Grace, 2010 and Minudasht, 37°10′N 55°30′E, 2♂♂, Müller, 2012). October 2012. Plant association: Polylectic with a General distribution: Algeria, preference for Fabaceae (Banaszak and Caucasus, Cyprus, Iran, Morocco, Romasenko, 1998; Grace, 2010 and Northern Asia, South eastern- and Müller, 2012), Vicia (Fabaceae), Borago Central-Europe, Tunisia, Turkey officinalis (Boraginaceae) (Khodaparast (Banaszak and Romasenko, 1998; and Monfared, 2012 and 2013). Grace, 2010; and Müller, 2012). 19. Osmia (Osmia) cornuta (Latreille, Plant association: Oligolectic on 1805) Brassicaceae (Banaszak and Material examined: Mazandaran Romasenko, 1998 and Müller, 2012). province, Qaemshahr, 36°28′N 52°52′E, 17. Osmia (Helicosmia) caerulescens 1♀, August 2014. (Linnaeus, 1758) General distribution: Algeria, Cyprus, Material examined: Mazandaran Egypt, Europe, Iran, Tunisia, province, Sari, 36°30′N 53°30′E, 1♀, Turkmenistan, Turkey (Banaszak and 2♂♂, June 2013. Romasenko, 1998; Grace, 2010 and General distribution: Algeria, Canada, Müller, 2012). China, Cyprus, Egypt, Europe, India, Plant association: Polylectic; prefers Iran, Jordan, Kazakhstan, Kyrgyzstan, Rosaceae (Westrich, 1989; Banaszak Morocco, Syria, Tajikistan, Tunisia, and Romasenko, 1998 and Amiet et al., Turkey, Turkmenistan, USA and 2004). Uzbekistan (Banaszak and Romasenko, 20. Osmia (Helicosmia) dimidiata 1998; Grace, 2010 and Müller, 2012). Morawitz, 1870 Plant association: Polylectic, prefers Material examined: Golestan province, Fabaceae, Lamiaceae, Boraginaceae and Gonbad, 37°30′N 55°00′E, 1♀, 2♂♂, Antirrhineae (Banaszak and September 2013. Romasenko 1998; Grace, 2010 and General distribution: Asia minor, Müller, 2012), Vicia sp. (Fabaceae), Caucasus, Cyprus, Iran, Morocco, Borago officinalis (Boraginaceae), Kyrgyzstan, Lebanon, Palestine, South Medicago sativa (Fabaceae), Euphorbia Europe, Turkey and Turkmenistan sp. (Euphorbiaceae), Epilobium hirsutum (Banaszak and Romasenko, 1998; (Onagraceae) (Khodaparast and Grace, 2010 and Müller, 2012). Monfared , 2012, and 2013). Plant association: Probably oligolectic 18. Osmia (Pyrosmia) cephalotes on Asteraceae, visiting Cirsium syriacum, Morawitz, 1870 Calendula persica, Centaurea hyalolepis, Material examined: Mazandaran Statice sinuata, Echium sericeum, province, Amol, 36°28′N 52°21′E, 2♀♀, Scolymus hispanicus and Marrubium 1♂, April 2013; Golestan province, vulgare apolum (Grace, 2010 and Gorgan, 36°50′N 54°30′E, 2♀♀, July Müller, 2012). 2009. 21. Osmia (Helicosmia) melanogaster General distribution: Algeria, Spinola, 1808 Caucasus, Cyprus, Iran, Jordon, Libya, Morocco, Palestine, South- and Eastern-

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Material examined: Mazandaran General distribution: Albania, Algeria, province, Qaemshahr, 36°28′N 52°52′E, China, Cyprus, Egypt, France, Greece, 1♂, August 2014. Corsica, Crete, Iran, Italy, Jordan, General distribution: Algeria, Morocco, Palestine, Portugal, Sardinia, Caucasus, Cyprus, Egypt, Iran, Jordan, Sicily, Spain, Syria, Turkey, Libya, South, Eastern and Central Turkmenistan and Ukraine (Grace, 2010 Europe, Morocco, Palestine, Syria, and Müller, 2012). Tunisia and Turkey (Banaszak and Plant association: Oligolectic on Romasenko, 1998; Grace, 2010 and Asteraceae (Müller, 2012). Müller, 2012). Upon the results of this research Plant association: Oligolectic on together with other works on Carduoideae (Asteraceae) (Müller, Megachilidae of Northern Iran (e.g. 2012). Tavakkoli et al., 2010 and Nadimi et al., 22. Osmia (Helicosmia) niveata 2013 a, b and 2014) indicate that there is (Fabricius, 1804) a diverse fauna of these beneficial Material examined: Golestan province, in northern Iran. Although the fauna of Gonbad, 37°30′N 55°00′E, 1♀, 1♂, Megachilidae of southern Iran was September 2013. studied rather well (see references) but General distribution: Cyprus, Europe, the fauna of northern Iran was poorly Iran, Jordan, Lebanon, Northern Africa, studied so far. Regarding to the diverse Palestine, Syria, Turkey, Turkmenistan flora in northern Iran, we expect much (Grace, 2010 and Müller, 2012). more species of Megachilidae in the Plant association: Oligolectic on mentioned area. The megachilids are Asteraceae with a distinct preference for important pollinators of several Carduoideae (Westrich, 1989; Amiet et wildflowers, vegetables and fruits, and al., 2004 and Müller, 2012). are used as pollinators by commercial 23. Osmia (Allosmia) rufohirta growers of blueberries, onions, carrots Latreille, 1811 and alfalfa (Bohart, 1972 and Pitts-Singer Material examined: Mazandaran and Cane, 2011). In addition to the province, Sari, 36°30′N 53°30′E, 1♀, species diversity of Iranian Megachilidae, June 2013. there are many other unknown data such General distribution: Algeria, as the diversity of nesting biology and Caucasus, China, Jordan, Morocco, floral relationships. Diverse materials are South, Central and Eastern Europe, Syria, used in nest building and the inclusion of Turkmenistan, Tunisia and Turkey these foreign materials in nest (Banaszak and Romasenko, 1998; construction may have promoted a Grace, 2010 and Müller, 2012). massive range expansion and Plant association: Polylectic with a diversification within the family (Cane et preference for Fabaceae (Banaszak and al., 2007; Litman et al., 2011 and Romasenko, 1998 and Müller, 2012). Gonzales et al., 2012). Also, many 24. Osmia (Helicosmia) signata insects (e.g. Chrysididae, Mutillidae, Erichson, 1835 Formicidae, Rhipiphoridae, Meloidae, Material examined: Mazandaran Cleridae, etc.) attack the nests of province, Amol, 36°28′N 52°21′E, 2♀♀, leafcutting bees (Ahmed Khattaby, 1992 April 2013. and Woodward, 1994), which determining of these natural enemies can

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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (1): 398 - 408 be an interesting research work in Comba, L. and Comba, M. (1991): different regions of Iran. Catalogo Degli Apoidei Laziali Acknowledgements (Hym.; Aculeta). Fragmenta We thank C. Eardley (South Entomologica, 82: 1-117. Africa) and A. Müller (Switzerland) for Dorn, M. and Weber, D. (1988): Die their helpful suggestions, J. Rastegar Luzerne- Blattschneiderbiene und (Iran) for loaning some specimens, S. ihre Verwandten in Mitteleuropa, Ungericht (Switzerland) and J. Straka Megachile rotundata u. A. Die (Czech Republic) for providing some Neue Brehm- Bücherei, Mit 56, papers. This research was supported by Abbildungen und 1 Farbtafel, p Islamic Azad University. 112. References Ebadi, R. (1995): Collection, Ahmed Khattaby, A.M. (1992): Studies identification and preliminary study on the common enemies of family of pollinator fauna in Megachilidae (Hymenoptera) in Esfahan province. Proceedings of Egypt. Ph. D Dissertation of 12th Iranian Plant Protection Zagazig University, Egypt. Congress, p. 309. Amiet, F.; Hermann, M.; Müller, A. Engel, M. S. (2006): A new species of and Neumeyer, R. (2004): Apidae Osmia from Iran (Hymenoptera: 4: Anthidium, Chelostoma, Megachilidae). Acta Entomologica Coelioxys, Dioxys, Heriades, Slovenica, 14: 123-130. Lithurgus, Megachile, Osmia, Esmaili, M. and Rastegar, R. (1974): Stelis. Fauna Helvetica, 9: 1-273. Identified species of Aculeate Banaszak, J. and Romasenko, L. Hymenoptera of Iran. Journal of the (1998): Megachilid Bees of Entomological Society of Iran, 2 Europe. Pedagogical University of (1): 41-52 [in Persian]. Bydgoszcz, Poland, pp 239. Gonzalez, V.H.; Griswold, T.; Praz, Bohart, G.E. (1972): Management of C.J. and Danforth, B.N. (2012): wild bees for the pollination of Phylogeny of the family crops. Annual Review of Megachilidae (Hymenoptera: Entomology, 17: 287-312. Apoidea) based on adult Bosch, J. and Blas, M. (1994): Foraging morphology. Systematic behaviour and pollinating Entomology, 37: 261-286. efficiency of Osmia cornuta and Grace, A. (2010): Introductory Apis mellifera on almond biogeography to bees of the Eastern (Hymenoptera, Megachilidae and Mediterranean and Near East. Apidae). Applied Entomology and Bexhill Museum Association, pp Zoology, 29: 1-9. 283. Cane, J.H., Griswold, T.L. and Parker, Güler, Y. and Çağatay, N. (2006): F.D. (2007): Substrates and Faunistic study on Megachilini, materials used for nesting by North Osmiini and Anthidiini tribes American Osmia bees (Apiformes: (Hymenoptera: Megachilidae) in Megachilidae). Annals of the Central Anatolia. Journal of Entomological Society of America, Entomological Research Society, 100: 350-358. 8(2): 15-34.

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