Turkish Journal of Zoology Turk J Zool (2014) 38: 444-459 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1309-5

Distribution data on the family Melittidae (Hymenoptera) of Turkey with considerations about their importance as pollinators

Hikmet ÖZBEK* Department of Plant Protection, Faculty of Agriculture, Atatürk University, Erzurum, Turkey

Received: 13.10.2013 Accepted: 10.01.2014 Published Online: 20.05.2014 Printed: 19.06.2014

Abstract: The examination of specimens collected from various parts of Turkey, mainly from East Anatolia, and an overview of the literature allows us to reach the conclusion that the Melittidae of Turkey are represented by 3 genera, Dasypoda (14 species), Macropis (2 species), and Melitta (9 species), with a total of 25 species including Dasypoda toroki Michez, 2004, a new record for the Turkish fauna. Dasypoda hirtipes (Fabricius, 1793), Melitta (Melitta) leporina (Panzer, 1799), and M. dimidiata Morawitz, 1876 are the most widespread and abundant species. Dasypoda friesana Schletterer, 1890; D. longigena Schletterer, 1890; D. patinyi Michez, 2002; D. visnaga (Rossi, 1790); Melitta rasmonti Michez, 2007; M. nigricans Alfken, 1905; M. singular Michez, 2012; M. haemorrhoidalis; and M. melanura (Nylander, 1852) are very rare species and most are known from one locality only. The rest of the species are moderately distributed in Turkey. Five species of Dasypoda and 3 species of Melitta have type localities from Anatolia; of these, D. longigena, M. bicollaris, M. singular, M. rasmonti, and D. warnckei are endemic to Anatolia. New distribution areas were added for each species and the plant species visited were included. Although the genus Dasypoda visits mostly wild flowers, D. hirtipes also frequently visits sunflowers and it is an important pollinator of this plant. In the case of the genus Macropis, females collect oil and pollen from the flowers of Lysimachia (Primulaceae) as larval food. Melitta leporina, M. dimidiata, and M. bicollaris are important pollinators of fodder crops, such as alfalfa, sainfoin, and various clover species and some other legumes.

Key words: Hymenoptera, Melittidae, Dasypoda, Macropis, Melitta, fauna, new record, pollinator, Turkey

1. Introduction Members of this rather small family are found Bees are in the Apiformes group of Apoidea (Hymenoptera), primarily in temperate regions of the northern hemisphere which is a diverse group of pollen-eaters comprising and Africa, the greatest number of genera and species approximately 18,000 described species (Michener, 2007; being found in warm xeric areas. Maximal diversity Michez et al., 2009). They occur in most ecosystems occurs in southern Africa, where all 3 subfamilies occur. where they are usually the most important pollinators, The Palearctic region also supports a moderate number and therefore they play a key role in ecosystem function of species and genera. In the Nearctic region the family is rare, unknown in tropical America and Australia, as well (O’Toole, 1993; Waser and Ollerton, 2006). Currently, 9 as in the Indo-Malayan area (Michener, 2007; Michez et bee families are recognized, and Melittidae is one of the al., 2009). smallest bee families with more than 200 species in 14 Michener (1981) divided the Melittidae into 3 genera (Engel, 2005; Michener, 2007; Michez et al., 2009, subfamilies: Meganomiinae, Dasypodainae, and 2012). Melittinae. Dasypodainae and Melittinae occur in Turkey The family Melittidae includes short-tongued bees. and Meganomiinae is known from Africa and Arabia only Michener (2007) emphasized that no single character is (Michener, 1981), whereas, according to Engel (2001), the unique to Melittidae, although the combination of a short, Melittidae are subdivided into 4 subfamilies: Dasypodainae, pointed glossa and unspecialized first 2 segments of the Macropidinae, Meganomiinae, and Melittinae. labial palpus with a slender, V-shaped lorum; tapering The Dasypodainae are relatively species-rich, mentum; and elongate, fully exposed middle coxa as in comprising more than 100 species in xeric areas of both long-tongued bees separates the Melittidae from other the Old World and the Nearctic region (Michener, 2007; short-tongued bee families. Michez et al., 2009, 2010). Dasypoda is the only widespread

* Correspondence: [email protected] 444 ÖZBEK / Turk J Zool genus, which occurs from the temperate to the xeric areas Erzurum, Dasypoda pyriformis tubera from İçel (Mersin), of the Palearctic, including Turkey. Dasypoda determines and D. braccata anatolica from Konya. Recently, additional the northern limit of the Dasypodainae to 62°N (Michez species were described from Turkey: Dasypoda warnckei et al., 2004a). The other Dasypodainae genera, Capicola Michez, 2004 from Kayseri; Melitta rasmonti Michez, Friese, 1911; Eremaphanta Popov, 1940; Hesperapis 2007 from Hakkari; and M. singular Michez, 2012 from Cockerell, 1898; and Samba Friese, 1908, are each endemic Nevşehir (Michez et al., 2004a, 2012; Michez and Eardley, in different Old World and Nearctic semideserts (Michez 2007). Local researcher Özbek (1976, 1979, 1980, 2008, and Pauly, 2012). The Melittinae comprise 4 genera: Melitta 2011) highlighted the importance of various Melitta Kirby, 1802; Macropis Panzer, 1809; Rediviva Friese, 1911; species on the pollination of different fodder crops, such and Redivivoides Michener, 1981 (Michener, 1981). Melitta as alfalfa, sainfoin, and red clover. and Macropis have Holarctic distributions; Melitta is the The aim of this paper is to present the latest knowledge of most widespread and probably one of the most diverse, the Turkish Melittidae bees, their geographic distribution, while Rediviva and Redivivoides are endemic in Africa plant species visited, and biogeographical affinities. The (Michener, 2007; Michez and Eardley, 2007). Two genera, present contribution is based on material collected from Macropis and Melitta, occur in Turkey. various parts of Anatolia by the author and his colleagues Some important studies have been conducted on since the 1960s and literature data. Melittidae in the Palearctic: Quilis (1928) reviewed the Spanish species of Dasypoda. The West Palearctic region 2. Materials and methods of Melittidae was studied by Warncke (1973), who listed Most of the bee specimens were collected by sweeping 17 Melitta species including 4 new species and several with an insect net from various habitats in different subspecies, 3 Macropis species, and 18 Dasypoda species localities, mainly in eastern Anatolia, since the 1960s. The including 1 new species and several subspecies. The catches of bees were made during the flowering periods of Melittidae species of China and Dasypoda species of plants, between April and September. In addition to bees, European Russia were studied by Wu (1978) and Radchenko the flowering plants that particular bee species visited and Pesenko (1989), respectively. An annotated account of were noted or the samples were picked. Identification of the species of Dasypoda was provided by Baker (2002), who the bees was verified by comparison with the preserved described D. litigator from Iran. Michez (2002) described specimens, which were determined by the late K Warncke, D. patinyi from Syria. In a phylogenetic study, Michez et al. late YA Pesenko, and B Tkalcu at the Entomology Museum (2004b) recognized 4 subgenera. Michez and Pauly (2012) of Erzurum, Turkey (EMET). Additionally, the keys described D. riftensis from Ethiopia. This species was the provided by Warncke (1973) and Michez et al. (2004a) first record of the genus Dasypoda in sub-Saharan Africa. were followed. Certain undetermined specimens were Most of the genera in Melittidae were revised: Michez determined by D Michez. Host-plant data were based on et al. (2004a) revised the West Palearctic Dasypoda and the field records and labels of pinned specimens of EMET. recognized 28 species, including 4 new species. Michez The material mentioned in this study was deposited in the and Eardley (2007) provided an overview of the literature collection of EMET, along with a few specimens deposited and their examination of many specimens from various in the collection of the American Museum of Natural collections, including type materials, enabled the first History (AMNH). monographic revision of the genus Melitta. They listed 43 species, including 2 new ones in the 2 subgenera Melitta s. 3. Results str. and Cilissa. More recently, Michez et al. (2012) described The examination of the specimens collected from various 4 Melitta species. Michez and Patiny (2005) revised the oil- parts of the country and an overview of the literature allow collecting bee genus Macropis Panzer and described a new us to reach the conclusion that the Melittidae of Turkey are species from Laos. Other revisional studies included those represented by 3 genera, Dasypoda (14 species), Macropis on Capicola Friese (Michez et al., 2007a), Eremaphanta (2 species), and Melitta (9 species), with a total of 25 Popov (Michez and Patiny, 2006), Hesperapis Cockerell species. (Stage, 1966; Michener, 1981), Promelitta Warncke 3.1. Genus Dasypoda Latreille, 1802 (Michez et al., 2007b), Meganomia Cockerell (Michener, The genusDasypoda is characterized by the presence 1981), and Rediviva Friese (Whitehead et al., 2008). of only 2 submarginal cells on the fore wing and a well- Studies on the family Melittidae in Turkey are very developed scopa of the female hind leg, black body, vertex restricted. Warncke (1973) presented a catalog and key elevated, no basitibial plate (Michener 1981; Michez et al., for 38 West Palearctic species. Among them, 15 species (1 2004a, 2004b). Michez et al. (2004b) described 4 subgenera Macropis, 8 Dasypoda, and 6 Melitta species) were indicated based on morphological cladistic analysis: Dasypoda s. st.; to occur in Turkey. He described Melitta bicollaris from Heterodasypoda Michez, 2004; Microdasypoda Michez,

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2004; and Megadasypoda Michez, 2004. The diversity 14.09.1978, ♀, leg. H. Özbek, det. H. Özbek; Başaklı, centers of each of the 4 subgenera are restricted to 1 of the 01.09.1988, 4 ♀♀, leg. H. Özbek, det. H. Özbek; Kayaaltı, following parts of the Mediterranean region: the Balkans, 800 m, ♂, leg. G. Tozlu, det. D. Michez and W. Thayse; Morocco, and Spain (Michez and Pauly, 2012). Michez Olur, Coşkunlar, 12.07.1991, ♂, leg. H. Özbek, det. H. (2005) listed 33 Dasypoda species that are common in the Özbek; Pasinler, center, 12.07.1980, ♂, leg. H. Özbek, det. Palearctic region from Portugal and the Canary Islands B. Tkalcu; 01.08.1983, ♂, leg. H. Özışık, det. D. Michez to Japan, although most species are West-Palearctic and and W. Thayse; Rabat, 2200 m, 13.06.1996, ♀, leg. H. especially abundant in the Mediterranean basin. Özbek, det. H. Özbek; Şenkaya, Gaziler, 1650 m, 2 ♀♀, 3.1.1. Dasypoda (Dasypoda) hirtipes (Fabricius, 1793) leg. R. Kotan, det. H. Özbek; Tortum, Aksu, 16.09.1977, ♀, Distribution: Whole of Europe; Asia from Turkey to leg. H. Özbek, det. H. Özbek, Aksu, 1450 m, 19.07.2003, Mongolia and China; North Africa (Warncke, 1973; Wu, ♂, ♀, leg. S. Çoruh, det. H. Özbek, det. D. Michez and W. 1978; Michez et al., 2004a, 2004b). In Turkey: Amasya, Thayse; Bağbaşı, 20.09.1978, 41 ♂♂, 4 ♀♀, leg. H. Özbek, Balıkesir, Bursa, İstanbul, Kastamonu, Konya, Kütahya, det. B. Tkalcu and H. Özbek; Şenkaya, Turnalı, 03.09.1990, Nevşehir, Samsun, and Sinop (Warncke, 1973). ♀, ♂, leg. E. Yıldırım, det. H. Özbek. Eskişehir: Sivrihisar, Material: Ağrı: Patnos, 28.07.1978, ♀, 15 ♂♂, 13.08.1990, ♀, leg. H. Özbek, det. H. Özbek. Iğdır: Aralık, leg. H. Özbek, det. B. Tkalcu and H. Özbek. Ankara: 02.08.1997, ♂, leg. B. Gül, det. D. Michez and W. Thayse. Şereflikoçhisar, 08.07.1998, 2 ♂♂, leg. C. Güçlü, det. D. İzmir: Menemen, 900 m, 17.06.1994, ♂, leg. H. Özbek, det. Michez and W. Thayse.Ardahan : Center, 11.08.1976, ♂, Michez and W. Thayse. Kars: Digor, 1770 m, 17.07.2005, leg. H. Özbek, det. B. Tkalcu; Posof, center, 28.08.1991, ♂, leg. H. Özbek, det. D. Michez and W. Thayse; Sarıkamış, leg. H. Özbek, det. H. Özbek; Sarıdarı, 28.08.1991, ♀, leg. E. 11.08.1983, 2 ♂♂, leg. H. Özbek, det. Y. A. Pesenko and Yıldırım, det. H. Özbek; Türközü, 28.08.1991, 5 ♀♀, 3 ♂♂, H. Özbek. Kayseri: Develi, 25.06.1980, 2 ♀♀, 3 ♂♂, leg. leg. H. Özbek, det. H. Özbek, D. Michez and W. Thayse. H. Özbek, det. H. Özbek. Manisa: Alaşehir, 23.07.1990, 2 Artvin: Yusufeli, İşhan, 17.09.1978, ♀, leg. H. Özbek, det. ♂♂, ♀, leg. H. Özbek, det. H. Özbek. Samsun: 27.08.1981, B. Tkalcu; İşhan, 15.08.1991, 2 ♀♀, leg. E. Yıldırım, det. 2 ♂♂, leg. O. Ecevit, det. H. Özbek. Sivas: Suşehri, H. Özbek; Sarıgöl, 700 m, 05.07.1994, ♂, leg. H. Özbek, 07.07.1999, 2 ♂♂, leg. H. Özbek, det. H. Özbek. Tokat: det. as D. altercator (Harris). Bilecik: Center, 600 m, ♂, leg. Center, 19.08.1992, 3 ♀♀, leg. H. Özbek, det. H. Özbek; E. Yıldırım, det. D. Michez and W. Thayse. Bitlis: Tatvan, 900 m, 19.08.1992, ♂, ♀, leg. H. Özbek, det. D. Michez and Nemrut Dağı, 23.07.2003, ♀, leg. H. Özbek, det. H. Özbek. W. Thayse. Van: Edremit, 29.07.1978, 15 ♀♀, 7 ♂♂, leg. H. Erzincan: Çatalarmut, 09.08.1990, 3 ♂♂, leg. E. Yıldırım, Özbek, det. B. Tkalcu and H. Özbek; Gevaş, 29.07.1978, ♀, det. H. Özbek; Kemah, Alp, 19.07.1997, ♀, leg. H. Özbek, leg. H. Özbek, det. H. Özbek; Kuzgunkıran, 29.07.1978, ♀, det. H. Özbek; Üzümlü, Karakaya, 31.07.1991, 3 ♂♂, leg. leg. H. Özbek, det. H. Özbek. Yozgat: Yerköy, 09.08.1989, E. Yıldırım, det. Y. A. Pesenko as D. altercator; Tercan, 3 ♂♂, leg. H. Özbek, det. H. Özbek. Yazıören, 29.06.1980, ♂, leg. H. Özbek, det. Y. A. Pesenko. Plants associated: Sunflower (Helianthus annuus L.) Erzurum: Atatürk University Campus, 12.07.1970, ♂, leg. and safflower (Carthamus tinctorius L.) are important H. Özbek, det. K. Warncke; 24.07.1978, ♂, leg. H. Özbek, cultivated plant species that are frequently visited by D. det. B. Tkalcu; 18.08.1967, ♂ leg. O. Ecevit, det. H. Özbek; hirtipes. Wild plants: Apiaceae: Ammi visnaga (L.) Lam., 20.08.1966, ♂, leg. H. Özbek, det. K. Warncke; 22.08.1968, A. majus L., Daucus carota L., Eryngium billardierei ♂, leg. H. Özbek, det. H. Özbek; 01.08.1990, ♀, leg. K. F.Delaroche, E. bithynicum Boiss., E. creticum Lam., Gümüş, det. H. Özbek; Eşkinkaya, 20.07.2003, ♀, ♂, leg. Ferula orientalis L., Heracleum spp., Pimpinella spp.; J. G. Rozen, H. Özbek, det. J. G. Rozen (American Natural Asteraceae: Achillea millefolium L., Arctium lappa L., History Museum, AMNH); Palandöken, 2100 m, ♂, leg. E. A. minus (Hill), Carduus acanthoides L., C. nutans L., Yıldırım, det. H. Özbek; Horasan, Karakoçan, 19.07.1990, 3 Centaurea drabifolia Sm., C. glastifolia L., C. iberica Trevir. ♂♂, leg. E. Yıldırım, det. H. Özbek; Köprüköy, 26.08.1991, ex Spreng., C. hyalolepis Boiss., C. macrocephala Muss. ♀, ♂ leg. H. Özbek, det. H. Özbek, D. Michez and W. Puschk., C. solstitialis L., Cichorium intybus L. (the most Thayse; Köprüköy, 19.07.1990, 2 ♂♂, leg. E. Yıldırım, det. favorable plant), Cirsium arvense (L.), C. lappaceum Y. A. Pesenko as D. altercator; Oltu, center, 20.07.1976, ♂, (M.Bieb), Echinops galaticus Freyn, E. orientalis Trautv., leg. H. Özbek, det. B. Tkalcu; 14–16.09.1978, 2 ♂♂, leg. Onopordum acanthium (L.), O. illyricum L., O. tauricum H. Özbek, det. B. Tkalcu; Anzav deresi, 31.08.1996, ♀, ♂, Willd., Pallenis spinosa (L.), Senecio spp., Taraxacum leg. G. Tozlu, det. H. Özbek; Ayvalı, 27.07.1990, ♂, leg. E. aleppicum Dahlst., T. phaleratum G.E.Haglund ex Rech., T. Yıldırım, det. Y. A. Pesenko as D. altercator; 26.08.1993, scaturiginosum G.E.Haglund, Tragopogon aureus M.Bieb.; ♀, leg. G. Tozlu, det. H. Özbek; Başaklı, 01.09.1978, 9 Convolvulaceae: Convolvulus arvensis L.; Dipsacaceae: ♂♂, leg. H. Özbek, det. Y. A. Pesenko as D. altercator; Cephalaria gigantea (Ledeb.), C. lycica Matthew, C. procera 07.09.1978, 4 ♂♂, leg. H. Özbek, det. H. Özbek; Başaklı, Fisch. & Avé-Lall.; Euphorbiaceae: Euphorbia orientalis

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L., Dipsacus laciniatus L., Scabiosa caucasica M.Bieb.; 3.1.3. Dasypoda (Dasypoda) tubera Warncke, 1973 Fabaceae: Melilotus officinalis L.; Lamiaceae: Salvia Distribution: Syria and Turkey. In Turkey: İçel and Hatay aethiopis L., S. candidissima Vahl, S. multicaulis Vahl, S. (Warncke, 1973); Çukurova (rather abundant), Amasya, sclarea L., S. verticillata L., S. viridis L., Satureja sp., Stachys Bilecik, Çorum, Eskişehir, İçel, İzmir, Hakkari, Hatay, annua L., S. cretica L., Thymus comptus Friv., T. leucostomus Taurus Mts. (Michez et al., 2004a). Hausskn. & Velen., T. sipyleus Bois.; Scrophulariaceae: Material: Adana: Akvatan, 22.05.1995, 2 ♂♂, leg. G. Verbascum spp. Çankaya, det. D. Michez, W. Thayse and H. Özbek. Antalya: Remark: Dasypoda hirtipes is the most widespread and Beydağları, Saklıkent yolu, Alimin Pınarı, 09.07.1991, abundant species of the genus in Turkey (Figure 1), as well 2 ♀♀, leg. H. Özbek, det. D. Michez, W. Thayse and H. as outside of Turkey. Özbek. İzmir: Menemen, 900 m, 17.06.1994, 2 ♀♀, ♂, leg. H. Özbek, det. D. Michez, W. Thayse and H. Özbek. 3.1.2. Dasypoda (Dasypoda) pyriformis Radoszkowski, Remark: Warncke (1973) described D. tubera from İçel 1887 (Mersin) as the subspecies of D. pyriformis on the basis of Distribution: Italy, Balkan Peninsula, Croatia, Macedonia, the male. Later, Michez et al. (2004a) found females and Albania, Bulgaria, Greece, Turkey (Michez et al., 2004a). additional males and described the male, and the status of Michez (2012a) noted that D. pyriformis is present in the D. tubera was revised at the species level. northeastern part of the Mediterranean basin. Most of the Plants associated: Carduus sp., Centaurea solstitialis, records are found in Greece. In Turkey: Denizli (Warncke, and Cichorium intybus. 1973); Amasya, as D. schlettereri Friese, 1900, which is a 3.1.4. Dasypoda (Dasypoda) warnckei Michez, 2004 synonym of D. pyriformis (Baker, 2002). Distribution: Turkey. Kayseri (type locality), Niğde, Material: Erzurum: Oltu, Başaklı, 01.08.1977, 2 Nevşehir, Çorum, Denizli, Hakkari, Kars (Michez at al., ♀♀ leg. H. Özbek, det. Y. A. Pesenko. Kars: Kağızman, 2004a). Kuloğlu, 1600 m, 01.08.2002, ♂, leg. M. Kesdek, det. D. Material: Iğdır: Bayraktutan, 40°00′949N, 43°55′105E, Michez and W. Thayse. 17.08.2005, ♀, ♂, leg. H. Özbek, det. D. Michez and W. New localities: Erzurum and Kars. Thayse.Kars : Digor, 1770 m, 17.07.2005, ♂, leg. H. Özbek, Remark: Dasypoda pyriformis is a rare species det. H. Özbek. occurring in Turkey. It is a Mediterranean species; among Plants associated: Cichorium intybus, Onopordum sp. Asian countries, it occurs only in Turkey (Amasya). In the Remark: As far as is known, D. warnckei is endemic present study it has been recorded from Erzurum and Kars to Turkey. It is not abundant, although it is a rather provinces, and Kars is its easternmost distribution record, widespread species from east to west (Figure 1). However, both in Turkey and the world. it is remarkable to note that although I have made Plants associated: Carduus sp., Centaurea glastifolia L., intensive collections within Erzurum Province, I have not Cichorium intybus. encountered this species so far in Erzurum.

D. pyriformis D. tubera D. warnckei D. pyrotrichia D. argentata D. braccata D. friesana D. longigena D. patinyi D. spinigera D. aurata Mersin D. toroki D. visnaga D. hirtipes Figure 1. Distribution of the genus Dasypoda in Turkey.

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3.1.5. Dasypoda (Heterodasypoda) pyrotrichia Förster, leg. H. Özbek, det. Y. A. Pesenko. Bayburt: Demirdöven, 1855 30.07.1992, ♀, leg. H. Özbek, det. H. Özbek; Kopdağı, Distribution: Portugal, Spain, France, Greece, Bulgaria, 10.08.1991, 2 ♀♀, 2 ♂♂, leg. H. Bostan, det. D. Michez Macedonia, Israel, Syria, and Turkey (Michez et al., 2004a). and W. Thayse; Kopdağı, 2400 m, 13.08.1977, 4 ♀♀, leg. In Turkey: D. pyrotrichia was described from Anatolia Ö. Çalmaşur, det. H. Özbek. Bingöl: Solhan, Bağlan, 2122 (Kleinasien) (Baker, 2002). It has already been recorded m, ♂, leg. M. Kesdek, det. H. Özbek. Erzincan: Kızıldağ, in Erzurum, Gümüşhane, Kars, Kayseri, and Trabzon 1800 m, 23.07.1991, 4 ♀♀, leg. H. Özbek, det. H. Özbek; (Michez et al., 2004a). Cevizli, 15.07.1982, ♂, leg. H. Özbek, det. K. Warncke; Material: Bayburt: Yaylapınar, 26.07.1992, ♀, leg. H. 26.07.1983, 3 ♀♀, ♂, leg. H. Özbek, det. B. Tkalcu and Bostan, det. H. Özbek. Erzincan: Cevizli, 26.07.1993, 2 H. Özbek. Erzurum: Gölet, 1950 m, 25.06.2003, ♀, leg. S. ♀♀, leg. H. Özbek, det. K. Warncke and Y. A. Pesenko. Çoruh, det. H. Özbek; Güngörmez, 2400 m, 05.08.1990, Erzurum: Atatürk University Campus, 10.06.2000, ♀, 7 ♂♂, leg. H. Özbek, det. Y. A. Pesenko and H. Özbek; leg. M. Kestek, det. H. Özbek; Ilıca, Ovacık, İspir road, Karagöbek Mts., 2200 m, 05.07.1989, ♂, leg. H. Özbek, det. 08.08.1990, ♂, leg. Ü. Avcı, det. D. Michez and W. Thayse; H. Özbek; Köşkköyü, 14.07.1992, ♀, leg H. Özbek, det. H. Köşkköyü, 14.07.1992, ♂, leg. H. Özbek, det. D. Michez Özbek; Şenyurt, 2300 m, 22.08.1991, 10 ♂♂, 6 ♀♀, leg. and W. Thayse; Köprüköy, Örentaş, 04.07.2004, ♀, leg. H. Özbek and E. Yıldırım, det. H. Özbek, D. Michez, and H. Özbek, det. H. Özbek; Oltu, Başaklı-Tutmaç border, W. Thayse; Kargapazarı, Radar road, 2100–2800 m, 20– 1700–2000 m, 02.07.2000, 15 ♀♀, 3 ♂ ♀, leg. H. Özbek 28.08.1989, 2 ♀♀, 14 ♂♂, leg. H. Özbek, det. H. Özbek and Ö. Çalmaşur, det. H. Özbek; Kaleboğazı, 28.07.1990, and Y. A. Pesenko; 11.08.1990, ♀, leg. H. Özbek, det. H. ♂, leg. E. Yıldırım, det. H. Özbek; Pasinler, Çalıyazı, Özbek; 24.08.1988, 15♀♀, leg. H. Özbek, det. H. Özbek; 13.07.1997, 9 ♂♂, leg. E. Yıldırım, det. H. Özbek; Rabat, Umudum plateau, 2100 m, 14.07.1990, 12 ♀♀, 10 ♂♂, 2400 m, 11.07.1996, 46 ♂♂, leg. E. Yıldırım, det. H. Özbek; leg. H. Özbek, det. H. Özbek; Umudum plateau, 2800 m, Pelitli, 14.07.1996, 2200 m, 14.07.1996, 2 ♀♀, 3 ♂♂, leg. 08.08.1991, 11 ♀♀, 8 ♂♂, leg. H. Özbek, det. H. Özbek, D. E. Yıldırım, det. H. Özbek; Şenkaya, Turnalı, 1800 m, Michez and W. Thayse; Uzunahmet, 03.08.1981, ♀, leg. H. 19.06.1991, ♀, leg. E. Yıldırım, det. D. Michez and W. Özbek, det. H. Özbek; Aşkale, 07.07.1980, 4 ♀♀, leg. H. Thayse; 06.07.1990,♀ , leg. E. Yıldırım, det. H. Özbek; Özışık, det. H. Özbek; Çat, 20.07.1989, ♀, leg. H. Özbek, Tortum, Aşağı Meydanlar, 04.07.1991, ♀, leg. H. Özbek, det. H. Özbek; Ilıca, Konaklı, 2200–2400 m, 22.07.2000, 5 det. D. Michez and W. Thayse; Doruklu Yaylası, 2000 m, ♀♀, 20 ♂♂, leg. H. Özbek, E. Yıldırım, Ö. Çalmaşur, det. 03.07.1991, ♀, 2 ♂♂, leg. H. Özbek, det. H. Özbek. Kars: H. Özbek; Narman, Kireçli Mt., 12.07.2000 m, ♂, leg. C. Sarıkamış, İssisu, 07.07.1991, 2 ♂♂, leg. E. Yıldırım, det. Güçlü, det. H. Özbek; Şehitler, 1600 m, 05.08.1997, 2♂♂, H. Özbek, det. D. Michez and W. Thayse. leg. E. Kılıç, det. H. Özbek; Olur, Oğuzkent, 22.08.1992, ♀, Plants associated: The samples were collected mainly leg. İ. Aslan, det. H. Özbek; Süngübayır, 20.08.1992, ♀, leg. from the edges of wooded areas on Helianthemum İ. Arslan, det. H. Özbek; Köprüköy, Örentaş, 04.07.2004, nummularium (L.) Mill. (Cistaceae). A few samples were leg. H. Özbek, det. H. Özbek; Süngübayır, 20.08.1992, ♀, collected from Onopordum sp., Cirsium sp., Cephalaria leg. İ. Aslan, det. H. Özbek; Oltu, Başaklı, 13.08.1977, ♀, procera, Melilotus alba, and Salvia spp. Michez et al. (2008) leg. H. Özbek, det. H. Özbek; 01.09.1978, 7 ♀♀, leg. H. mentioned that D. pyrotrichia appears strictly oligolectic Özbek, det. H. Özbek; Pasinler, Pelitli, 2200 m, 14.08.1996, on Cistaceae, although the sample was too small to reach a 5 ♂♂, 2 ♀♀, leg. E. Yıldırım, det. H. Özbek; Rabat, 2400 m, definite conclusion. 11.08.1996, 16 ♀♀, 46 ♂♂, leg. E. Yıldırım, det. H. Özbek; 3.1.6. Dasypoda (Megadasypoda) argentata Panzer, 1809 15.08.1995, 4 ♀♀, leg. H. Özbek, det. H. Özbek; Şenkaya, Distribution: It is widespread, particularly in western Soğanlı Pass, 2450 m, 04.08.2000, 2 ♀♀, leg. S. Çoruh, Europe, Spain, France, Austria, Germany, Switzerland, C. Güçlü, det. H. Özbek; Turnalı, 1750 m, 25.07.1996, ♂, Italy, Poland, Bohemia, Slovakia, Croatia, Hungary, leg. E. Yıldırım, det. D. Michez and W. Thayse; Turnalı, Romania, Lithuania, Armenia, Azerbaijan, European 06.08.1988, ♂, leg. E. Yıldırım, det. Y. A. Pesenko; Turnalı, Russia, Macedonia, Sweden, Bulgaria, Greece, Ukraine, 25.08.1991, 3 ♀♀, leg. E. Yıldırım, det. H. Özbek; Turnalı, Caucasus, Georgia. In Asia: Turkey, Kazakhstan, India, 2000 m, 01.09.1988 4 ♀♀, ♂, leg. E. Yıldırım, det. H. Iran, Iraq, and Syria. In Africa: Algeria, Egypt, Tunisia Özbek and Y. A. Pesenko. Kars: Sarıkamış, 26.08.1991, 2 (Warncke, 1973; Michez et al., 2004a, 2004b). In Turkey: ♀♀, leg. H. Özbek, det. H. Özbek. Bayburt, Erzurum, Gümüşhane, İçel (Warncke, 1973); Remark: Radchenko and Pesenko (1989) preferred Hakkari, Erzincan, Sivas (Michez et al., 2004a). using D. thoracica Baer, 1853 for this species, although Material: Ağrı: Tahir Mt., 25.07.1978, ♂, leg. H. none of the specialists accepted changing D. argentata Özbek, det. Y. A. Pesenko. Ardahan: Göle, 10.08.1977, 5 (Michez et al., 2004a) except for Celary (2002). It is a ♂♂, leg. Özbek, det. Y. A. Pesenko and H. Özbek; 3 ♂♂, widespread species and is very abundant, particularly

448 ÖZBEK / Turk J Zool in East Anatolia. After D. hirtipes it is the second most Remark: Warncke (1973) described the subspecies D. widespread species of the genus Dasypoda both in Turkey braccata anatolica from Konya and Sivas. (Figure 1) and the world. Plants associated: Achillea millefolium, Ammi Plants associated: Daucus carota, Eryngium billardierei, visnaga, Daucus carota, Eryngium billardierei, Cephalaria Cichorium intybus, Echinops galaticus, E. orientalis, gigantean, C. lycica, C. procera, Scabiosa argentata, S. Onopordum acanthium, O. tauricum, Tragopogon aureus, caucasica, Carduus acanthoides, C. nutans, Cichorium Cephalaria gigantea, C. lycica, C. procera, Euphorbia intybus, Cirsium arvense, Echinops galaticus, Onopordum orientalis, Dipsacus laciniatus, Scabiosa caucasica, Melilotus acanthium, O. illyricum. It is particularly associated with officinalis, and Salvia aethiopis. It is remarkable to note the genus Cephalaria (Dipsacaceae). that D. argentata shows high preference to the Cephalaria 3.1.8. Dasypoda (Megadasypoda) frieseana Schletterer, species; in particular, C. procera is the most frequently 1890 visited plant. Distribution: Greece, Macedonia, and Turkey (Warncke, 3.1.7. Dasypoda (Megadasypoda) braccata Eversmann, 1973). In Turkey: İçel (Warncke, 1973). 1852 Material: Bayburt: Demirözü, 12.07.1992, 2 ♂♂, Distribution: Albania, Austria, Bulgaria, Greece, Caucasus, leg. H. Özbek, det. H. Özbek; 30.07.1992, 2 ♀♀, 6 Italy, Macedonia, Serbia, European Russia, Hungary, ♂♂ leg. H. Özbek, det. D. Michez, W. Thayse and H. Poland, Ukraine, Kazakhstan, and Turkey (Warncke, 1973; Özbek; 30.07.1992, ♀, ♂, leg. H. Bostan, det. H. Özbek; Radchenko, 1987; Michez et al., 2004a, 2004b). In Turkey: 31.07.1992, ♀, 4 ♂♂, leg. H. Bostan, det. H. Özbek; 11 ♂♂, Konya, Sivas (Warncke, 1973); Ankara, Kahramanmaraş, ♀♀ Konya, Niğde, Malatya, Elazığ, Erzincan, Kars, Mardin, 3 , leg. H. Özbek, det. D. Michez, W. Thayse and H. Sivas (Michez et al., 2004a). Özbek; 14.08.1992, 3 ♂♂, leg. H. Bostan, det. H. Özbek; Material: Bayburt: Demirözü, 31.07.1992, Bayrampaşa, 31.07.1992, ♀, 2 ♂♂, leg. H. Bostan, det. H. Bayrampaşa, 31.07.1992, ♀, leg. H. Bostan, D. Michez, and Özbek. W. Thayse; Demirözü, 30.07.1992, ♂, leg. H. Bostan, det. Remark: Warncke (1973) noted that D. friesana was D. Michez and W. Thayse; Kopdağı, 10.08.1991, ♀, leg. H. previously known from Turkey (İçel). However, Baker Bostan, det. H. Özbek; Yaylapınar, 26.07.1992, ♂, leg. H. (2002) and Michez et al. (2004a) gave the Balkan Peninsula Bostan, det. H. Özbek. Erzincan: Cevizli, 26.07.1983, 2 (Akarnanien) as the only distribution area of this species, ♀♀, leg. H. Özbek, det. H. Özbek. Erzurum: DSİ Gölet, and in the distribution map that was prepared by Michez 25.06.2003, ♀, leg. S. Çoruh, det. H. Özbek; Güngörmez, et al. (2004a), only Greece and Macedonia were marked. 2300 m, 05.08.1990, 7 ♀♀, leg. H. Özbek, det. H. Özbek; Recording this species from northeastern Anatolia is Karagöbek, 28.07.1990, ♀, leg. E. Yıldırım, det. H. Özbek; very important under these circumstances. D. frieseana Kargapazarı, Radar road, 2800 m, 24.08.1988, 12 ♀♀, is recorded in Turkey as well as from the Asian continent leg. H. Özbek, det. H. Özbek; Konaklı, 2000–2400 m, for the first time with the present study and Bayburt is the 22.07.2000, ♀, leg. E. Yıldırım, det. H. Özbek; Şenyurt, easternmost record of this species (Figure 1). 2300 m, 22.08.1991, 5 ♀♀, leg. H. Özbek and E. Yıldırım, Plants associated: Arctium lappa, Cephalaria gigantean, det. H. Özbek; Umudum plateau, 2800 m, 08.08.1991, C. procera, and Dipsacus laciniatus. ♂ , leg. H. Özbek, det. D. Michez and W. Thayse; Aşkale, 3.1.9. Dasypoda (Megadasypoda) longigena Schletterer, 07.07.1980, 5 ♀♀, leg. H. Özışık, det. H. Özbek; Kopdağı, 1890 2200–2400 m, 13.08.1997, 3 ♀♀, leg. Ö. Çalmaşur, det. H. Distribution: Dasypoda longigena was described from Özbek; Oltu, Başaklı, 13.08.1977, ♀, 01.09.1978, 4 ♀♀, leg. Anatolia (Kleinasien) by Schletterer (1890). Later it was H. Özbek, det. H. Özbek; Sütkans, 1500 m 25.06.1996, ♀, recorded from Erzurum (Warncke, 1973; Michez and leg. E. Yıldırım, det. D. Michez and W. Thayse; Pasinler, Patiny, 2002; Michez et al., 2004a). With the present Rabat, 15.08.1995, ♂, leg. E. Kılıç, det. D. Michez and W. Thayse; Rabat, 2200 m, 15.08.1995, 2 ♂♂, leg. İ. Aslan, det. knowledge it can be seen that D. longigena is endemic to D. Michez and W. Thayse; Oltu, Başaklı-Tutmaç border, Anatolia. 1700–2000 m, 02.07.2000, 13 ♀♀, leg. H. Özbek, det. H. Remark: Dasypoda longigena is one of the earliest bee Özbek; Şenkaya, Turnalı, 25.07.1996, ♂, leg. E. Yıldırım, species described from Anatolia. It was virtually extinct in det. D. Michez and W. Thayse; Turnalı, 28.07.1993, ♂, leg. Anatolia and had not been recorded for over 80 years, the E. Yıldırım, det. H. Özbek; 2000 m, 02.09.1988, 5 ♀♀, leg. first record after its description being in 1973 by Warncke E. Yıldırım, det. H. Özbek; Tortum, Doruklu plateau, 2000 (1973) and only in Erzurum. It is remarkable that in spite m, Uzundere, Dikyar, 02.07.1994, ♀, leg. İ. Aslan, det. H. of intensive collections in Erzurum and neighboring Özbek. Hakkari: Kaval Valley, 1300 m, 20.07.1982, ♂, ♀, provinces since the 1970s it has not been encountered; it is leg. W. Deprins, det. D. Michez and W. Thayse. probably extinct or on the verge of extinction.

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3.1.10. Dasypoda (Megadasypoda) patinyi Michez, 2002 Remark: Although D. visnaga has a very large Distribution: Syria, Turkey (Michez, 2002; Michez et al., distribution range throughout the Mediterranean 2004a). So far it has been recorded in Turkey only from countries, including North Africa, more recently it has Şanlıurfa (Michez et al., 2004a). been recorded solely from Antalya in Turkey (Figure 1). Remark: Michez (2002) described D. patinyi from 3.2. Genus Macropis Panzer, 1809 Suwaydan (Syria), which is not far from Şanlıurfa. Dasypoda Macropis is the most distinctive genus of Melittinae; the patinyi is represented by only one female (Şanlıurfa, front wing has 2 submarginal cells, the face of the male 37°08′N, 38°46′E, 01.06.1968, leg. J. Gusenleitner) in Turkey. is yellow, and there is a well-developed pygidial plate in both sexes (Michener, 1981). Oil-collecting bees are found 3.1.11. Dasypoda (Megadasypoda) spinigera Kohl, 1905 worldwide and always in association with particular oil- Distribution: Caucasus, Armenia, Iran, Bulgaria, Greece, producing flowers (Bassin et al., 2011). The oil-collecting Macedonia, Italy, Romania, Ukraine, Turkey (Warncke, and transporting structure of Macropis features short, 1973; Michez et al., 2004a); former Russia (Radchenko and Pesenko, 1989). In Turkey: Kayseri (type locality), Aksaray, dense, velvety hairs on the small segments of all the Ankara, Aydın, Bitlis, Çanakkale, İçel, Konya, Nevşehir, tarsi for collecting the oil and the broad hind tibia and Niğde, Sivas, Van, Tekirdağ (Warncke, 1973; Baker, 2002; basitarsus with fine, dense, plumose scopal hairs for oil Michez et al., 2004a). transport (Michener, 2007). All females of the Macropis Material: Erzincan: Ilıç, 15.07.1994, ♀, leg. H. Özbek, species collect oil and pollen from flowers ofLysimachia det. D. Michez and W. Thayse. Erzurum: Köprüköy, (Primulaceae) as larval food (Rozen and Jacobson, 19.07.1990, ♂, leg. Ş. Güçlü, det. H. Özbek. Konya: Selçuk 1980; Cane et al., 1983; Michez and Patiny, 2005). Since University Campus, 14.07.1997, 6 ♀♀, 5 ♂♂, leg. F. Aydın, Lysimachia produces no nectar, adults of Macropis visit det. D. Michez, W. Thayse, and H. Özbek.Van : Edremit, other flowers for their own energy needs (Pekkarinen et 19.07.1978, ♀, leg. H. Özbek, det. B. Tkalcu. al., 2003; Michez and Patiny, 2005). Plants associated: Cephalaria gigantea, C. procera, Macropis includes 16 species in three subgenera: Scabiosa argentata, S. caucasica, and Echinops galaticus. Paramacropis Popov and Guiglia, 1936; Sinomacropis 3.1.12. Dasypoda (Megadasypoda) aurata Rudow, 1881 Michener, 1981; and Macropis Panzer s. str., occurring Synonyms: Dasypoda spectabilis Rudow, 1881; D. mixta in the eastern Palearctic, in China, and in the Holarctic Radoszkowski, 1887; D. thomsoni Schletterer, 1890; D. region including Turkey, respectively (Michez and Patiny, suripes (Christ, 1791). 2005). Distribution: Bohemia, Sweden, Denmark, Germany, 3.2.1. Macropis (Macropis) frivaldszkyi Mocsary, 1878 Austria, Italy, Poland, Moravia, Slovakia, Hungary, Croatia, Distribution: Italy, Bulgaria, Kazakhstan, Macedonia, Macedonia, Albania, Romania, Bulgaria, Lithuania, Romania, Greece, Croatia, Hungary, Serbia, and European Greece, Belarus, Ukraine, Armenia, Cyprus, European Russia. In Turkey: Erzurum (Warncke, 1973); Ankara, Russia, Turkey (Warncke, 1973; Michez et al., 2004a). In Turkey: Aydın, Hatay, İçel, Muğla (Michez et al., 2004a); Konya, Hakkari, Van (Michez and Patiny, 2005); Sinop Erzurum as D. mixta Radoszkowski, 1887 (Baker, 2002; (Bassin et al., 2011) (Figure 2). Michez et al., 2004a) (Figure 1). Material: Erzurum: Atatürk University Campus, 12.07.1970, ♀, leg. H. Özbek, det. K. Warncke. 3.1.13. Dasypoda (Megadasypoda) toroki Michez, 2004 Distribution: Israel, Syria (Michez et al., 2004b). Plants associated: Lysimachia vulgaris L. (Primulaceae). Material: Antalya: Kumluca, 08.05.1998, 3 ♀♀, leg. G. 3.2.2. Macropis (Macropis) fulvipes (Fabricius, 1805) Tozlu, det. H. Özbek. Şanlıurfa: Karaköprü, 16.06.1992, ♂, Distribution: Europe (except in the United Kingdom, leg. R. Hayat, det. D. Michez and W. Thayse. Sweden, and Norway), Georgia, Russia, Algeria (Warncke, Remark: D. toroki was recently described from Israel 1973; Michez and Patiny, 2005; Bassin et al., 2011). In (Michez et al., 2004b). In the present study it has been Turkey: Çankırı, Kastamonu, Artvin, Ardahan, and Rize recorded from Antalya and Şanlıurfa. Antalya is the (Michez and Patiny, 2005); Kastamonu and Sinop (Bassin westernmost distribution record of this species (Figure 1). et al., 2011) (Figure 2). It is a new record for the Turkish fauna. Plants associated: Pekkarinen et al. (2003) noted that Plants associated: Carduus sp. Macropis bees are apparently all oligolectic on Lysimachia; 3.1.14. Dasypoda (Megadasypoda) visnaga (Rossi, 1790) females collect pollen and oil from Lysimachia, whereas Distribution: Mediterranean countries from the Atlantic nectar is usually collected from a wide variety of host coast of Portugal to the Aegean coast of Turkey including plants. Michez et al. (2008) emphasized that, in the North Africa (Algeria, Morocco, and Tunisia). In Turkey: Palearctic region, Macropis bees are specialized on the Antalya (Michez, 2012a). subgenus Lysimachia.

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Macropis frivaldszkyi Macropis fulvipes Melitta nigricans M. bicollaris M. budensis M. dimidiata Mersin M. haemorrhoidalis M. melanura M. rasmonti M. singular M. leporina Figure 2. Distribution of the genera Macropis and Melitta in Turkey.

3.3. Genus Melitta Kirby, 1802 Distribution: Palearctic. Widespread in Europe The Melitta species superficially resemble the species of including southern Sweden and Finland. In Asia, known Andrena (Andrenidae), although their scopae are limited from Anatolia and Iran, Kyrgyzstan to Mongolia (Warncke, to the hind tibia and basitarsus (no flocculus). Like other 1973; Michez and Eardley, 2007). In Turkey: Erzurum Melittidae, they have a short tongue with all segments of (Warncke, 1973; Özbek, 1976, 1979, 1980). the labial palpus similar to one another, one subantennal Material: Afyon: Sultandağı, 25.06.1995, ♂, leg. H. suture, and no facial foveae. There are 3 submarginal ♀♀ cells (the 3rd is longer than the 2nd) in the forewing, no Özbek, det. H. Özbek. Aksaray: Center, 27.06.1975, 4 , yellow markings and mainly brownish to blackish pilosity, 2 ♂♂, leg. H. Özbek, det. H. Özbek. Amasya: Merzifon, widened apical tarsi, lateral tubercles on the labrum, apical 23.07.1998, ♂, leg. H. Özbek, det. H. Özbek. Artvin: projection on the posterior basitarsus, and volsella with Yusufeli, 1350 m, 22.07.2003, 3 ♀♀, leg M. Kesdek, det. elongated digitus. In the male, the seventh sternum has a H. Özbek; Cinnar, 15.07.1992, 2 ♂♂, leg. E. Yıldırım, large disk and weakly developed lateral process (Michener, det. H. Özbek. Bilecik: Center, 21.06.1978, 3 ♂♂, leg. H. 1981; Michez et al., 2009). Özbek, det. H. Özbek. Bursa: Uludağ, 20.06.1978, ♀, 3 The genus Melitta occurs in the Palearctic, in southern ♂♂, leg. H. Özbek, det. H. Özbek. Erzincan: Çağlayan, and eastern Africa, and in the Nearctic regions (Warncke, 39.56670_39.65000, 06.07.2001, ♂, leg. J. G. Rozen and 1973; Michener, 1981; Eardley and Kuhlmann, 2006). It H. Özbek, det. D. Michez. Erzurum: Atatürk University is most diversified in the Palearctic region (Michener, Campus, 39.90250_41.23500, 2000 m, 07.06.2007, ♂, leg. 2007). It is rich in species, although morphologically monotonous compared to other melittid bees (Michez et J. S. Ascher, H. Özbek and J. G. Rozen, det. J. S. Ascher; al., 2009). 28.06.1978, ♂, leg. H. Özbek, det. H. Özbek; 28.06.2001, ♂, Warncke (1973) recognized 3 subgenera of Melitta leg. J. G. Rozen and H. Özbek, det. D. Michez; 30.06.2007, (Cilissa, Melitta s. str., and Pseudocilissa) based on the ♀, leg. J. S. Ascher, H. Özbek, J. G. Rozen, det. J. S. Ascher; revision of West Palearctic species. Michez and Eardley 17.07.2010, 4 ♀♀, leg. J. S. Ascher, H. Özbek, det. J. S. (2007) reviewed the literature and examined many Ascher; 21.07.2010, 2 ♀♀, ♂; 29.07.2010, ♂, leg. J. S. specimens from various collections (including the type Ascher, H. Özbek, J. G. Rozen, det. J. S. Ascher; 10.07.2001, material); they produced the first monographic revision ♀, leg. H. Özbek, J. G. Rozen, det. D. Michez; 17.07.2003, of the genus Melitta and noted that there are currently 2 ♀♀, ♂, leg. J. G. Rozen and H. Özbek, det. D. Michez; 48 valid species. However, very recently, Dellicour et al. 18.07.2003, 2 ♀♀, leg. J. G. Rozen and H. Özbek, det. D. (2014) described 2 more Melitta species, and so it rose to Michez (in AMNH); 19.07.1987, ♂, leg. R. Hayat, det. H. 50 species. Özbek; 21.07.2003, 3 ♀♀, leg. J. G. Rozen and H. Özbek, 3.3.1. Melitta (Melitta) leporina (Panzer, 1799) det. D. Michez; 12.07.1970, 2 ♀♀, leg. H. Özbek, det. K. Synonyms: Apis leporina Panzer, 1799; Andrena fortipes Warncke; 12–15.07.1971, 12 ♀♀, leg. H. Özbek, det. K. Imhoff, 1832; Cilissa ruthenica Radoszkowski, 1891; Warncke; 20–26.07.1971, 10 ♀♀, leg. H. Özbek, det. K. Melitta centaureae Torka, 1922 Warncke and H. Özbek; 17–22.07.1974, 5♀♀, leg. H.

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Özbek, det. K. Warncke; 29.07.1974, 4 ♀♀, leg. H. Özbek, Turkey. Wild plants: Fabaceae: Astragalus aduncus Willd., det. K. Warncke; 20–29.07.2003, 10 ♀♀, leg. H. Özbek, A. aureus Willd., A. baibutensis Bunge, A. bicolor Lam., det. H. Özbek; İspir, 15.07.1991, ♀, leg. H. Özbek, det. K. A. christianus L., A. galegiformis L., A. lagurus Willd., Warncke; İspir, Kan, 20.07.1970, ♀, leg. H. Özbek, det. K. A. longifolius Lam., A. onobrychis L., A. ponticus Pall., Warncke; Oltu, 4 km WSW of Oltu, 40.53305_41.98527, Coronilla orientalis Mill., C. varia L., Glycyrrhiza glabra 1500 m, 03.07.2001, 2 ♂♂, leg. J. G. Rozen and H. Özbek, L., Hedysarum elegans Boiss. & A.Huet, H. nitidum Willd., det. D. Michez; 30.06.1980, ♀, leg. H. Özbek, det. K. Lathyrus spp., Lotus corniculatus L., Medicago falcata L., Warncke; 04.07.1974, 4 ♀♀, leg. H. Özbek, det. K. Warncke M. lupulina L., M. papillosa Boiss., Melilotus alba Desr., M. and H. Özbek; 08–11.07.1974, 36 ♂♂, leg. H. Özbek, det. officinalis (L.) Desr., Onobrychis armena Boiss. & A.Huet., H. Özbek; 9.07.1970, 2 ♀♀, 2 ♂♂ leg. H. Özbek, det. K. O. cana Boiss., Trifolium ambiguum M.Bieb., T. montanum Warncke and H. Özbek; 12–20.07.1970, 8 ♀♀, 4 ♂♂ leg. L., Vicia cracca L., and V. villosa Roth. H. Özbek, det. K. Warncke; 14–11–17.07.1974, 25 ♂♂, leg. Celary (2006) described the nesting ecology of M. H. Özbek, det. H. Özbek; 18.07.1970, 2 ♂♂, leg. H. Özbek, leporina. The female builds its nest in hard, clayed soil. det. H. Özbek; 18.07.1972, 2 ♂♂, leg. H. Özbek, det. H. They are not gregarious and the entrance to each nest is Özbek; 20.07.1971, 7 ♂♂, leg. H. Özbek, det. H. Özbek; concealed by vegetation. 23.07.1974, leg. H. Özbek, det. H. Özbek; 24.07.1970, ♀, 3.3.2. Melitta (Melitta) nigricans Alfken, 1905 leg. H. Özbek, det. K. Warncke; 26–28.07.1972, 9 ♀♀, leg. Distribution: Widespread in Europe from Portugal H. Özbek, det. H. Özbek; 26.07.1966, ♀, leg. H. Özbek, to Poland and Orenburg (Russia). Absent in England det. K. Warncke; 29.07.1970–74, 5 ♂♂, leg. H. Özbek, det. and Sweden, one record from Morocco and Argentina K. Warncke; Kandilli, 29.06.1970, ♂, leg. H. Özbek, det. (Warncke, 1973; Michez and Eardley, 2007). In Turkey: H. Özbek; Olur, Coşkunlar, 12.07.1991, ♀, leg. E. Yıldırım, Balıkesir (Warncke, 1973). det. H. Özbek; Oltu, 20.07.1970, 4 ♂♂, leg. H. Özbek, det. H. Özbek; 19.08.1987, ♀, ♂, leg. H. Özbek, det. H. Özbek; Remark: Although M. nigricans is a common species Tortum, Pehlivanlı, 12.07.1992, ♂, leg. E. Yıldırım, det. D. distributed throughout Europe, except for Fenno- Michez. Eskişehir: Sivrihisar, 13.08.1990, 2 ♂♂, leg. H. Scandinavia, it is very rare in Turkey, known only in Özbek, det. H. Özbek. Iğdır: Aralık, 02.08.1997, 4 ♂♂, Balıkesir (Figure 2). leg. B. Gül, det. H. Özbek. İzmir: Bornova, 08.07.1979, Plants associated: Michez et al. (2008) gave the family ♀, ♂, leg. H. Özbek, det. H. Özbek. Kayseri: Develi, Lythraceae as the host plants of M. nigricans. 27.06.1975, 5 ♀♀, 3 ♂♂, leg. H. Özbek, det. H. Özbek. 3.3.3. Melitta (Cilissa) bicollaris Warncke, 1973 Kütahya: Tavşanlı, 28.06.1979, ♂, leg. H. Özbek, det. H. Distribution: Warncke (1973) described the female of M. Özbek. Manisa: Salihli, 05.06.1989, ♀, leg. H. Özbek, det. bicollaris from Erzurum. Later, Michez and Eardley (2007) H. Özbek. Karaman: Center, 02.07.1975, 2 ♀♀, 4 ♂♂, leg. described the male based on a pair of specimens collected M. Kesdek, det. H. Özbek. Konya: Güneysınır, Gürağaç, from Erzurum. So far it has been known only from Artvin, 1017 m, 23.06.1999, ♀, leg. M. Kesdek, det. H. Özbek. Erzincan, Erzurum, and Kars provinces (Figure 2). With Nevşehir: Ürgüp, 28.06.1975, 2 ♀♀, 3 ♂♂, leg. H. Özbek, the present data it is endemic to East Anatolia. det. H. Özbek. Niğde: Çamardı, 29.06.1975, 3 ♀♀, 2 ♂♂, Material: Erzurum: Atatürk University Campus, leg. H. Özbek, det. H. Özbek. Samsun: Kavak, 26.07.1999, 09.07.1976, 2 ♀♀, leg. H. Özbek, det. H. Özbek; 15.07.1972, 2 ♀♀, ♂, leg. H. Özbek, det. H. Özbek. Sinop: Gerze, 2 ♀♀, leg. H. Özbek, det. K. Warncke; 13.07.1972, 5 ♀♀, 13.07.1998, ♀, 3 ♂♂, leg. H. Özbek, det. H. Özbek. Sivas: leg. H. Özbek, det. K. Warncke and H. Özbek; 18.07.1972, Hafik, 17.06.2001, ♂, leg. H. Özbek, det. H. Özbek. Van: 5 ♀♀, 11 ♂♂, leg. H. Özbek, det. H. Özbek; 28.07.1972, Muradiye, 38.99000_43.76000, 1750 m, 16.07.1988, ♀, 10 ♀♀, leg. H. Özbek, det. H. Özbek (all samples on O. leg. Schmid-Egger, det. K. Warncke (in AMNH). Yozgat: viciifolia); 2000 m, 39.90250_41.23500, 02.07.2002, ♂, Akdağmadeni, 08.07.2003, ♂, leg. H. Özbek, det. H. leg. J. G. Rozen and H. Özbek, det. D. Michez; Umudum Özbek. plateau, 2200 m, 14.07.1990, 12 ♀♀, leg. H. Özbek and Ş. Remark: M. leporina is the most widespread species for Güçlü, det. H. Özbek; Tortum, Pehlivanlı, 12-29.07.1992, the genus; it occurs from England to Vladivostok and from 2 ♀♀, leg. E. Yıldırım, det. D. Michez; Şenkaya, Turnalı, Finland to Spain (Michez, 2010). It is also one of the most 06.07.1990, 2 ♂♂, leg. E. Yıldırım, det. H. Özbek. widespread and abundant bee species occurring in Turkey Plants associated: Astragalus aduncus, A. bicolor, A. (Figure 2). gummifer, A. lagurus, A. ponticus, Hedysarum elegans, Plants associated: Melitta leporina visits alfalfa Lotus corniculatus, Medicago papillosa, M. sativa, Melilotus (Medicago sativa L.), sainfoin (Onobrychis viciifolia Scop.), alba, M. officinalis, Onobrychis cana, O. cf. stenostachya, red clover (Trifolium pratense L.), and white clover (T. O. transcaucasica, O. viciifolia, Medicago sativa, Trifolium repens L.), which are important fodder crops growing in montanum, T. repens, and Vicia cracca.

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3.3.4. Melitta (Cilissa) budensis (Mocsary, 1878) growing mainly in the East and Central Anatolian regions Distribution: Hungary, Russia, Ukraine, Armenia, of Turkey. Wild plants: Astragalus aduncus, A. bicolor, Kazakhstan, Turkey (Warncke, 1973; Michez and Eardley, A. cylindraceus, A. gummifer, A. lagurus, A. ponticus, 2007). In Turkey: Bolu (Warncke, 1973); Bitlis, Bolu, Hedysarum elegans, H. nitidum, Lotus corniculatus, Erzurum, Hakkari (Michez and Eardley, 2007) (Figure 2). Medicago papillosa, M. sativa, Melilotus alba, M. officinalis, Plants associated: Vicia cracca (Michez and Eardley, Onobrychis altissima, O. arenaria, O. araxina, O. cana, 2007). O. cornuta, O. transcaucasica, Ononis spinosa, Trifolium 3.3.5. Melitta (Cilissa) dimidiata Morawitz, 1876 ambiguum, T. montanum, Vicia alpestris, V. cracca. Synonyms: Cilissa robusta Radoszkowski 1876, Cilissa 3.3.6. Melitta (Cilissa) haemorrhoidalis (Fabricius, 1775) dimidiata hungaria Mocsary 1883, Pseudocilissa robusta, Synonyms: Andrena haemorrhoidalis Fabricius, Radoszkowski (1891). 1775; Cilissa haemorrhoidalis (Fabricius, 1775); Apis Distribution: South and East Europe as far as Central dichroa Gmelin, 1790; M. chrysura Kirby, 1802; M. Asia (Warncke, 1973; Michez and Eardley, 2007). Some haemorrhoidalis nigra (Friese, 1885); M. haemorrhoidalis isolated populations in England (Baker, 1965). In Turkey: frisica Zimmermann, 1935; M. haemorrhoidalis flavidorsis Ankara, Bitlis, Erzurum, İçel, Konya (Warncke, 1973; Ruszkowski, 1988 Özbek, 1979, 2011) (Figure 2). Distribution: Armenia, Austria, Belgium, Bohemia, Material: Erzurum: Atatürk University Campus, Bulgaria, Czech Republic, Denmark, Estonia, European 02.06.1974, ♀, leg. H. Özbek, det. H. Özbek; 04.06.1970, Russia, France, Finland, Germany, Georgia, Greece, 2 ♀♀, ♂, leg. H. Özbek, det. H. Özbek and K. Warncke; Hungary, Italy, Latvia, Lithuania, Luxembourg, Moravia, 08.22.06.1970, 55 ♂♂, 16 ♀♀, leg. H. Özbek, det. K. Netherlands, Norway, Poland, Romania, Slovakia, Warncke and H. Özbek; 09.06.1970, ♂, leg. H. Özbek, det. Slovenia, Spain, Sweden, Switzerland, Ukraine, United K. Warncke; 24.06.1970, 2 ♀♀, leg. H. Özbek, det. H. Özbek; Kingdom (Michez, 2012b). Although M. haemorrhoidalis 20.06.1971, 6 ♀♀, leg. H. Özbek, det. H. Özbek; 30.06.197, is one of the most common and widespread Melittidae 2 ♀♀, leg. H. Özbek, det. H. Özbek; 02–20.07.1970, 3 ♀♀, species in Europe, recently it was recorded in Rize ♂, leg. H. Özbek, det. H. Özbek; 06–26.07.1971, 48 ♂♂, (İkizdere, 40.78333_40.55) by Michez (2012b) (Figure 2). 24 ♀♀, leg. H. Özbek, det. H. Özbek and K. Warncke; 02– Plants associated: Michez and Eardley (2007) recorded 29.06.1974, 39 ♂♂, ♀, leg. H. Özbek, det. H. Özbek and B. M. haemorrhoidalis mainly on Campanula latifolia, C. Tkalcu; 01.07.1972, 3 ♂♂, leg. H. Özbek, det. H. Özbek; persicifolia, C. rapunculoides, C. rotundifolia, and C. 06.07.1976, ♂, leg. H. Özbek, det. H. Özbek; 12.07.1970, trachelium (Campanulaceae); Malva moschata and M. ♀, leg. H. Özbek, det. H. Özbek; 16.07.1966, 2 ♀♀, leg. H. sylvestris (Malvaceae). Özbek, det. H. Özbek; 11.07.1967, ♂, leg. H. Özbek, det. B. 3.3.7. Melitta (Cilissa) melanura (Nylander, 1852) Tkalcu; 17.07.1972, 3 ♀♀, leg. H. Özbek, det. H. Özbek and Synonyms: Kirbya melanura Nylander, 1852; Cilissa B. Tkalcu; 20.07.1971, 3♀♀, leg. H. Özbek, det. B. Tkalcu; wankowiczi Radoszkowski, 1891; Melitta wankowiczi 26.07.1974, ♀, leg. H. Özbek, det. H. Özbek; 10.06.2000, (Radoszkowski, 1891). 3 ♂♂, leg. M. Kesdek, det. H. Özbek; 03.07.1992, 5 ♀♀, Distribution: Austria, Belarus, European Russia, ♂, leg. E. Yıldırım, det. H. Özbek; Umudum plateau, Greece, Germany, Lithuania, Mongolia, Poland, Romania, 2200 m, 14.07.1990, 2100 m, 2 ♂♂, leg. Ş. Güçlü, det. D. Slovakia, Sweden, Ukraine, Turkey (Michez, 2012b). Michez; 08.08.1991, ♂, leg. H. Özbek, det. D. Michez; Although M. melanura is widespread in the Palearctic 2200 m, 14.07.1991, 2 ♂♂, leg. Ş. Güçlü and E. Yıldırım, from Austria to Mongolia, in Turkey it has been recorded det. D. Michez; İspir, 15.06.1971, ♂, leg. H. Özbek, det. only in Kars so far (Figure 2). It is represented only by H. Özbek; Oltu, center, 25.06.1971, 2♀♀, leg. H. Özbek, one specimen [1♀, Kars, Sarıkamış (40.33°N, 42.58°E), det. H. Özbek; 14.07.1972, 2 ♀♀, ♂, leg. H. Özbek, det. 06.08.1979 as M. wankowiczi (Radoszkowski, 1891)] H. Özbek; Başaklı, 15.07.1989, ♂, leg. H. Özbek, det. D. (Michez and Eardley, 2007). Michez; Şenkaya, Turnalı, 01.07.1990, ♂, leg. E. Yıldırım, 3.3.8. Melitta (Cilissa) rasmonti Michez, 2007 det. H. Özbek; Tekman, Yayla, 19.07.2005, 2450 m, ♂, C. Distribution: It was described in Hakkari, and one Güçlü, det. H. Özbek, Tortum, 14.07.1972, 3 ♀♀, ♂, leg. specimen was recorded in Erzurum (Palandöken, H. Özbek, det. H. Özbek; Uzundere, 28.06.1992, leg. M. 15.08.1978, ♀, leg. H. Özbek) (Figure 2). It is a mountain Atamanalp, det. H. Özbek. species; all materials were collected at an elevation of 2300 Plants associated: Medicago sativa, O. viciifolia, T. m or higher. pratense, T. repens. The present observations in the field 3.3.9. Melitta (Cilissa) singular Michez, 2012 and previous studies (Özbek, 1979, 2011) reveal that M. Distribution: only known from the type locality in Turkey dimidiata is one of the most important pollinators of (Kırşehir, Mucur, 1000 m, ♂, 25.06.1988, leg. K. Guichard) sainfoin (O. viciifolia), which is a valuable fodder crop (Figure 2). It is represented only by one specimen.

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4. Discussion Mediterranean, particularly the East Mediterranean basin. The examination of samples collected from various parts The Mediterranean is a vast, biologically rich region, of the country and an overview of the literature allow us to comprising Mediterranean ecosystems, arid and semiarid reach the conclusion that the Melittidae of Turkey comprise coastal and inland ecotones, and landscapes of faunistic 25 species in 3 genera: Dasypoda (14 species), Macropis (2 and floristic richness set in a geographically diverse mosaic. species), and Melitta (9 species). The Melittidae include The topography is varied, with many mountainous regions approximately 200 species in 14 genera (Michez et al., but also with low-lying plains and coastal strips. This could 2009, 2012) worldwide. With 25 species, Turkey is home explain the high diversity of plants and animals as well as to more than 12% of the world’s Melittidae. Among these Melittidae bees in Anatolia. I suggest that the speciation species, the most common and most frequently observed of most of these species occurred in the Mediterranean species across Turkey are Dasypoda hirtipes, D. argentata, basin, including Anatolia, and then dispersed to various D. braccata, Melitta leporina, and M. dimidiata. These directions. In their dispersal, apart from paleogeographic species are also widespread outside of Turkey; they have and paleoclimatic events, dispersal power (being large in Palearctic distribution. However, certain species are very size with a strong body structure) and the adaptive features rare and most are known from only 1 or 2 localities and of these species could play an important role. mainly from 1 locality, including D. friesana (from İçel and It is worth emphasizing that the current knowledge Bayburt), D. longigena (from Erzurum), D. patinyi (from on the distribution and fauna of the family Melittidae in Şanlıurfa), D. visnaga (from Antalya), Melitta nigricans Turkey is still incomplete. There are approximately 10 (from Balıkesir), M. haemorrhoidalis (from Rize), M. species known from only 1 locality each. Furthermore, rasmonti (from Erzurum and Hakkari), M. singular (from the occurrence of several species that are known to occur Kırşehir), and M. melanura (from Kars). Interestingly, M. in neighboring countries is suspected. In particular, the melanura and D. visnaga are widespread in the Palearctic, occurrence in Turkey of the following species seems likely although they have been recorded only from one locality or at least possible: Dasypoda litigator Bakker, 2002 and each. Additionally, M. melanura and M. singular are D. intermedia Michez, 2005 were recently described from represented only by one specimen each. Concerning new Iran; D. syriensis Michez, 2004 was described from Syria; records, D. toroki, recently described from Israel and Syria and D. cingulata Erichson, 1835 occurs in Mediterranean (Michez et al., 2004b), was recorded from Antalya and countries including Greece. I think that all of these species Şanlıurfa provinces. theoretically could occur in Turkey, although intensive Eight species (more than 30% of the Turkish melittids), collections must be conducted in various places, in 5 Dasypoda and 3 Melitta, have type localities from particular at the appropriate time of the year and on the Anatolia: Dasypoda tubera (İçel), D. warnckei (Kayseri), right host plant. D. longigena (Anatolia, locality uncertain), D. pyrotrichia 4.1. Melittidae bees as pollinators of cultivated and wild (Anatolia, locality uncertain), D. spinigera (Kayseri), plants Melitta bicollaris (Erzurum), M. rasmonti (Hakkari), and 4.1.1. Pollinators of crops M. singular (Kırşehir). Of these, D. longigena, D. warnckei, Mutualisms between insects and plants are widely M. bicollaris, M. singular, and M. rasmonti are endemic recognized as indispensable components in ecosystems to Anatolia (20% of the total species). Dasypoda spinigera functioning (Bronstein et al., 2006). Agricultural and D. pyrotrichia are quite widespread both in Turkey and pollination is the first indispensable step in a process that outside of Turkey. Dasypoda pyrotrichia has been recorded results in the production of fruits, vegetables, nuts, and mostly from the northeastern part of Anatolia. Michez seeds. Therefore, agriculture is highly dependent on insect (2012) pointed out that 3 subspecies of D. pyrotrichia are pollination (McGregor, 1976; O’Toole and Raw, 1991; recognized in 3 different areas around the Mediterranean Free, 1993; Cunningham et al., 2002; Woodcock, 2012; basin: Spain, Greece/Bulgaria, and Anatolia. Dasypoda Garibaldi et al., 2013). Bees are present in most ecosystems, longigena and D. friesana were described by Schletterer where they are primarily responsible for the pollination of (1890) from Turkey and Greece, respectively. No material flowering plants, playing a key role in ecosystems dynamics. has been found since the description of both of these It is a well-known fact that more than 35% of global crop species in Turkey. However, Warncke (1973) added new production depends on insect pollination. Most of these localities for D. friesana from Greece and Macedonia. pollinators are wild bees (Pedersen, 1961; Palmer-Jones Unfortunately, they appear to be either extinct or on the et al., 1966; Corbet et al., 1993; Kremen et al., 2002; verge of extinction in Turkey. Velthuis and Doorn, 2006; Klein et al., 2007; Garibaldi In general, when we take a look at the distribution et al., 2013). Wild bees are of enormous ecological and range of the Melittidae fauna of Turkey, all the economic importance as pollinators of many cultivated species occurring in Turkey are associated within the and wild plants and are thought to account for 75% of

454 ÖZBEK / Turk J Zool crop pollination requirements (Nabhan and Buchmann, bee species visiting sunflowers and constitutes the highest 1997); hence, they are often termed a keystone species percentage, Çalmaşur and Özbek (1999) reported that (O’Toole, 1993). Only a dozen bee species are managed many locally abundant bees contribute to pollination and for pollination worldwide (Kremen et al., 2002); in may be major pollinators. These researchers found that contrast, hundreds to thousands of the world’s more than of 42 bee species in the 5 families visiting sunflowers in 20,000 wild bee species contribute to crop pollination as Erzurum, honey bees accounted for approximately 80%, unmanaged populations (McGregor, 1976; Corbet et al., with wild bees representing 20%. Free (1993) noted that 1991; Free, 1993; Nabhan and Buchmann, 1997). It has although relatively few in number, solitary bees are the often been observed that alternative bee species are either most efficient pollinators of sunflowers. Whereas honey equally efficient or more efficient than the most widely bees often show little interest in collecting sunflower used managed pollinator, Apis mellifera L., in a variety of pollen, solitary bees often concentrate on doing so. crops (alfalfa, blueberry, red clover, cranberry, sunflower, Safflower is commercially cultivated for vegetable oil watermelon, tomato, and many more) (Parker et al., 1987; extracted from its seeds. It is now grown as an oil crop Kevan et al., 1990; Woodcock, 2012). in Turkey and some other countries. Boch (1961) caged Woodcock (2012) indicated that even plants that are 3 plots of safflowers to exclude bees and found that considered self-fertile can often realize a benefit in the they produced only approximately half as much seed as quantity or quality of production from cross-pollination, uncaged plots. He found that 90% of the insects visiting or even from the activity of insects moving pollen around safflowers were honey bees. Various researchers found on the flower that results in more grains being delivered. that, besides honey bees, different wild bee species visited Even in self-compatible plants, self-pollination is often an safflowers (Free, 1993). Eckert (1962) found that a self- “emergency mechanism” used by the plant to assure some fertile cultivar of safflowers set as much seed when caged reproduction if cross-pollination fails. Seeds and fruits to exclude insects as in the open (66: 64% set), although that develop as a result of self-pollination are often smaller a cultivar that was a somewhat self-sterile set less when and of lower quality than those resulting from cross- caged than in the open (41: 59% set). Dasypoda hirtipes pollination, because the plant will preferentially invest visits safflowers; it could be one of the efficient pollinators resources in cross-pollinated offspring and others may in favorable conditions in Turkey. even be aborted, reducing yield. Chicory, Cichorium intybus, is a light and refreshing Like many groups of phytophagous insects (Jaenike, vegetable used in salads and sandwiches; the flowers are 1990), bees show variation in host-plant use as well as host- also edible for salads and they can be frozen in ice cubes plant breadth. Whereas many bee species exhibit floral that are then added to iced tea. This plant is very abundant specificity, visiting only a restricted number of suitable and and widespread in Turkey, but cultivation might be very available plant taxa throughout their range (i.e. monolecty restricted. Most of the Dasypoda species, including D. or oligolecty), others display a wider spectrum of pollen tubera, D. warnckei, D. argentata, D. braccata, D. friesana, hosts (i.e. mesolecty or polylecty) (Michez et al., 2008). In and D. spinigera, and, in particular, D. hirtipes, visit C. general, when we examine the Melittidae species associated intybus flowers, from which they mostly collect pollen. with plant species, Dasypoda has a strong preference for It is evident from the present study that the genus the family Asteraceae, Melitta has a strong preference for Melitta is shown to be polylectic, although it exhibits Fabaceae, and Macropis is monolectic on Primulaceae. a clear preference for the family Fabaceae. Among Under these circumstances, as a family, Melittidae display the Melitta species, M. leporina, M. dimidiata, and M. a polylectic structure. bicollaris play an important role in the pollination of Among the cultivated plants, sunflower,Helianthus Fabaceae plants, such as alfalfa (M. sativa), sainfoin annuus, and safflower, Carthamus tinctorius, were visited (O. viciifolia), red clover (T. pratense), white clover (T. by D. hirtipes, D. pyriformis, and D. braccata. Particularly, repens), soybean (Glycine max L.), beans (Phaseolus spp.), D. hirtipes has been found to be the most intense and pea (Pisum sativum L.), chickpeas (Cicer arietinum L.), widespread species and frequently visits these plants. peanut (Arachis hypogaea L.), and licorice (Glycyrrhiza Different cultivars of sunflowers exhibit different degrees of glabra L.) (Free, 1993). Pollination has frequently been self-fertility. The isolated heads usually hold approximately the principal limiting factor in the growing of these 10%–20% seeds, compared with 70%–90% in exposed plants, particularly alfalfa and red clover, for seed. Field heads (Free, 1993). Observations and experiments on observations, especially in East and Central Anatolia, and the field scale confirm the value of bees in pollinating previous studies (Özbek, 1976, 1979, 2008) revealed that sunflowers and demonstrate that a shortage of bees may M. leporina is a valuable pollinator of alfalfa in Turkey. limit sunflower seed production (Free, 1993). Although The flower of alfalfa is peculiar, constructed so that the the honey bee (A. mellifera) is usually the most abundant staminal column is held under pressure within the keel

455 ÖZBEK / Turk J Zool by interlocking projections from the keel and wing petals. preference for sainfoin pollens and, while collecting the When the tension is released, the staminal column snaps pollens, pollinate about 90% of the flowers visited. The forward against the standard petal, causing the pollen to population of M. dimidiata is much larger than that of M. be distributed (Pedersen, 1961). This process is known as bicollaris, which has a distribution area restricted to the “tripping”, and once it has occurred, the staminal column eastern part of the country. Regarding sainfoin pollinators, does not return to the keel. Tripping is accomplished when M. dimidiata is the most abundant and widespread wild the keel is pressed down by the weight of a visiting bee bee; it visited 13–15 flowers per minute and foraged at (Pedersen, 1961; Özbek, 1979; Free, 1993). Individual 0600–1800 hours (Özbek, 1979). Among the wild bees it alfalfa plants range from being completely self-sterile or could be the best pollinator of sainfoin in Turkey. Although completely self-fertile, although more seeds are formed per it is slightly self-fertile, it is a cross-pollinated plant. pod from cross-pollination than from self-pollination and Clovers (Trifolium spp.) are also important crops with seeds from cross-pollination are larger (Free, 1993). Özbek high value as livestock forage, green manure, and cover (1979) found that in caged pods, setting was 5.48% and crops and also as honey plants in Turkey. Red clover seeds per pod were 1.42, while in exposed conditions they (T. pratense), white clover (T. repens), and alsike clover were 64.49% and 4.34, respectively. Although the relative (T. hybridum) are the major species growing in Turkey importance of honey bees and wild bees differs greatly (Açıkgöz, 2001). The flowers of clover follow the typical in different localities, a high proportion of honey bees legume structure, although the individual tubular flowers visiting alfalfa flowers fail to pollinate them, particularly are small, narrow, and grouped together in inflorescences. in locations where competing plants are abundant (Free, The anthers dehisce and release the pollen inside the bud 1993). I observed that honey bees rarely visit alfalfa flowers prior to opening. The weight of a flower visitor exerts and fail to collect pollen in Erzurum due to the abundance pressure on the standard and wing petals and causes the of other flowering plants such as O. viciifolia, Melilotus anthers and stigma to extend forward and press against the alba, M. officinalis, and T. repens in the area. Likewise, underside of the head of the visitor (Free, 1993). Following Özbek (1979) noted that wild bees were important in the a visit, in contrast to the alfalfa flower, the sexual structures pollination of alfalfa and listed 26 species visiting alfalfa return to their original position, allowing the same flower flowers in Erzurum Province. Later, in his countrywide to deliver pollen repeatedly (Bohart, 1957). The action of study, he found that approximately 150 species of bees in 5 insects is required for a successful seed set. Manipulation families of 30 genera visited alfalfa flowers in Turkey, which of the flowers causes pollen to be deposited on the ventral is located in the area where alfalfa supposedly originated surface of the pollinator bee at the same time that the (Özbek, 2008). Among the Melittidae species, M. leporina stigma is contacted and cross-pollen delivered. Although was one of the most efficient pollinators of alfalfa. It is the main pollinators of Trifolium spp., especially T. widespread in Turkey (Figure 2), active from sunrise to pratense, are various species of bumble bees and honey sunset during the flowering period and visiting 14–16 bees (Bohart, 1957; Palmer-Jones et al., 1966; Özbek, alfalfa flowers per minute. I made a field trip to Central 1980; Woodcock, 2012), M. leporina, M. dimidiata, and Anatolia, which is the main alfalfa seed-growing area of M. bicollaris visit T. pratense, T. repens, and T. hybridum. Turkey, to detect the activities and pollinating efficiency Field observations revealed that the presence of competing of M. leporina and make demonstrations in the field to the plants in the vicinity of clover-growing area caused visiting experts at the Agricultural Ministry. We observed together Melitta species to be less frequent. The main competing that it is very abundant in Central Anatolia and active plants are sainfoin (for M. dimidiata and M. bicollaris) and throughout the flowering period, efficiently pollinating alfalfa (for M. leporina). My impression is that T. repens is alfalfa flowers. The experts tracked the activities of M. more attractive for 3 of the Melitta species than the other leporina and revealed the importance of this bee in the Trifolium species. pollination of the alfalfa plant. Free (1993) noted that M. In conclusion, although the pollination of alfalfa, leporina is a particularly good alfalfa pollinator in some sainfoin, and clover species appear to present some other countries, such as Bulgaria, Denmark, France, difficulties, M. leporina is one of the most efficient Hungary, Poland, Sweden, and the former USSR. pollinators of alfalfa, although it is less attracted to sainfoin In contrast to M. leporina, 2 other Melitta species, M. and clover species. Melitta dimidiata and M. bicollaris, dimidiata and M. bicollaris, rarely visit alfalfa, especially and especially the former, are very efficient pollinators in the presence of sainfoin (O. viciifolia) and some other of sainfoin, although they are moderately important for competing plants such as Melilotus alba, M. officinalis, clover species. Furthermore, alfalfa is less attractive to M. Lotus corniculatus and T. repens in the surroundings. dimidiata and M. bicollaris. Field observations and my previous studies (Özbek, 1979, It is clear that increasing floral abundance and plant 2008) revealed that both of these species show a definite diversity reduced pollinator visitations to the target plants,

456 ÖZBEK / Turk J Zool suggesting competitive effects through both the quantity noted that Macropis bees are apparently all oligolectic on and diversity of resources. As pollinating agents of these Lysimachia. Females collect pollen and oil on Lysimachia, leguminous plants, in order to obtain more benefits whereas nectar is usually collected from a wide variety of from these bee species, efforts should be made to avoid host plants. competition with other flower species. Additionally, Concerning the Melitta species visiting wild plants, Melitta species mostly nest in field margins (Celary, 2006). the present data revealed that although Melitta species Therefore, in seed-growing areas, field margins, field edges visit various plant species in different families, they show a and paths, headlands, fence-lines, and nearby uncultivated clear preference for the family Fabaceae. In particular, M. patches of lands are important refuges for them. leporina and M. dimidiata are widespread and abundant 4.1.2. Pollinators of wild plants bees, visiting various wild plants in the Fabaceae. Among It is evident from this study and the literature data that, in them, Astragalus, Lotus, and Melilotus species have special addition to cultivated plants, the members of the family importance due to occurring in mountainous sloping Melittidae visit many wild plant species in the various areas, especially in eastern part of the country. These are plant families and pollinate them. In order to conserve important pasture plants for grazing domestic animals as and maintain biodiversity and to keep ecology in good well as wildlife. conditions, in addition to cultivated plants, wild plant Moreover, Melittidae species visit many plant species species also have to be pollinated at the optimum level. in different families. Turkey is a mountainous and hilly Furthermore, pollinator bees are indirectly responsible country. The average altitude is approximately 1250 m, and for the persistence of other guilds that depend upon floral more than 60% of the total land has more than 15% slopes. resources, such as herbivores and seed-eaters. Turkey is thus very sensitive to erosion and flood disasters. Dasypoda species show a large variation in the host- It is well known that plants provide protective cover on the plant choices. Michez et al. (2008) noted that most land and prevent soil erosion. Diversity of various plants Dasypoda species seem to be oligolectic on actinomorphic species is associated with many kinds of pollinators. The plant families (i.e. those with radiate symmetry). Dasypoda Melittidae include some of these pollinators. hirtipes is the most widespread and abundant species I should admit that in Turkey some farmers and even visiting different plant species in the families Apiaceae, agricultural experts are unaware of the importance of Asteraceae, Convolvulaceae, Dipsacaceae, Euphorbiaceae, bees as pollinators of crops and wild plants. Most of them Fabaceae, Lamiaceae, and Scrophulariaceae. Field rely on the honey bee alone (A. mellifera) for most crop observations and records reveal that it has a very strong pollination while the majority believe that wild bees are preference to C. intybus in nature; however, in various harmful insects, whereas, as we indicated previously, localities, it also forages exclusively on Cephalaria gigantea, pollinator bees are well known to provide key ecosystem C. procera, and Melilotus officinalis. Dasypoda pyriformis, services to both natural and agroecosystems. D. tubera, D. warnckei, D. toroki, and D. visnaga forage on various plant species in different families, although they Acknowledgments exclusively visit the plant species in the family Asteraceae I would like to thank Dr Denis Michez (Université de Mons, for pollen. D. argentata, D. braccata, D. frieseana, D. Laboratoire de Zoologie, Mons, Belgium) for determining longigena, and D. spinigera forage mainly on the plant certain specimens. I also thank all my colleagues, Osman species in the family Dipsacaceae, particularly the Ecevit, Şaban Güçlü, Rüstem Hayat, Erol Yıldırım, İrfan Cephalaria species. I observed that in mountainous areas Aslan, Göksel Tozlu, Önder Çalmaşur, Hidayet Bostan, of East Anatolia (Ağrı, Erzurum, and Kars provinces), Muhammed Atamanalp, Ümit Avcı, Engin Kılıç, Saliha above 2000 m, almost all the plants of C. gigantea and C. Çoruh, Memiş Kesdek, and Fatih Aydın, who helped me to procera host 1 or more of the above-mentioned Dasypoda collect certain bee samples in the field, and İrfan Çoruh for species. Among the 2 Macropis species occurring in determining plant species. I thank İbrahim Yücel Özbek, who Turkey, only 1 sample has been collected belonging to M. kindly prepared the distribution maps. I am also thankful to frivaldszkyi, from Lysimachia vulgaris. Michez et al. (2008) 2 anonymous reviewers for their helpful comments.

References

Açıkgöz E (2001). Yem Bitkileri. 3rd ed. Bursa, Turkey: Uludağ Baker DB (2002). A provisional annotated list of the nominal taxa Üniversitesi Güçlendirme Vakfı (in Turkish). assigned to the genus Dasypoda Latreille, 1802, with the description of an additional species (Hymenoptera: Apoidea, Baker DB (1965). Two bees new to Britain (Hymenoptera, Apoidea). Melittidae). Deut Entomol Z 49: 89–103. Entomologist’s Monthly Magazine 100: 279–286.

457 ÖZBEK / Turk J Zool

Bassin L, Alvarez N, Pellissier L, Triponez Y (2011). Ecological niche Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco overlap in sister species: how do oil-collecting bees Macropis R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, europaea and Macropis fulvipes (Hymenoptera: Melittidae) Afik O et al. (2013). Wild pollinators enhance fruit set of crops avoid hybridization and competition? Apidologie 42: 579–595. regardless of honey bee abundance. Science 340: 1608–1611. Boch R (1961). Honeybee activity on safflower (Carthamus tinctorius Jaenike J (1990). Host specialization in phytophagous insects. Annu L.). Can J Pl Sci 41: 559–562. Rev Ecol Syst 21: 243–273. Bohart GE (1957). Pollination of alfalfa and red clover. Annu Rev Kevan PG, Clark EA, Thomas VG (1990). Insect pollinators and Entomol 2: 355–380. sustainable agriculture. Am J Alternativ Agr 5: 13–22. Bronstein JL, Alarcón R, Geber M (2006). The evolution of plant- Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham insect mutualisms. New Phytol 1723: 412–428. SA, Kremen C, Tscharntke T (2007). Importance of pollinators in changing landscapes for world crops. P Roy Soc B 274: 303– Çalmaşur Ö, Özbek H (1999). Erzurum’da ayçiçeği (Helianthus 313. annuus L.)’ni ziyaret eden arı (Hymenoptera, Apoidea) türlerinin tespiti ve bunların tohum bağlamaya etkileri. Turk J Kremen C, Williams NM, Thorp RW (2002). Crop pollination from Biol 23: 73–89 (in Turkish). native bees at risk from agricultural intensification. PNAS 99: 16812–16816. Cane JH, Eickwort GC, Wesley ER, Spielholz J (1983). Foraging, grooming and mate-seeking behaviors of Macropis nuda McGregor SE (1976). Insect Pollination of Cultivated Crop Plants, (Hymenoptera, Melittidae) and use of Lysimachia ciliata Agriculture Handbook 496. Washington, DC, USA: US (Primulaceae) oils in larval provisions and cell linings. Am Department of Agriculture. Midl Natt 110: 257–264. Michener CD (1981). Classification of the bee family Melittidae with Celary W (2002). The ground-nesting solitary bee, Dasypoda a review of species of Meganomiinae. Contrib Am Entomol thoracica Baer, 1853 (Hymenoptera: Apoidea: Melittidae) and Institute 18: 1–135. its life history. Folia Biol-Prague 50: 191–198. Michener CD (2007). The Bees of the World. 2nd ed. Baltimore, MD, Celary W (2006). Biology of the solitary ground-nesting bee Melitta USA: Johns Hopkins University Press. leporina (Panzer, 1799) (Hymenoptera: Apoidea: Melittidae). J Michez D (2002). Dasypoda patinyi sp. nov. (Hymenoptera, Apoidea, Kans Entomol Soc 79: 136–145. Melittidae) espèce nouvelle recoltée en Syrie. Linz Biol Beitrage Corbet SA, Fussell M, Ake R, Fraser A, Gunson C, Savage A, Smith K 34: 737–742 (in French). (1993). Temperature and the pollinating activity of social bees. Michez D (2005). Dasypoda (Megadasypoda) intermedia sp. nov. Ecol Entomol 18: 17–30. (Hymenoptera, Apoidea, Melittidae), new species from Iran. Corbet SA, Williams IH, Osborne JL (1991). Bees and pollination of Zool Med Leiden 79: 123–127. crops and wild flowers in the European community. Bee World Michez D (2012a). Atlas of the European Bees: Genus Dasypoda. 72: 47–59. Mons and Gembloux, Belgium: STEP Project, Atlas Cunningham SA, FitzGibbon F, Heard TA (2002). The future of Hymenoptera. pollinators for Australian agriculture. Aust J Agr Res 53: 893– Michez D (2012b). Atlas of the European Bees: Genus Melitta. Mons 900. and Gembloux, Belgium: STEP Project, Atlas Hymenoptera. Dellicour S, Lecocq T, Kuhlmann M, Mardulyn P, Michez D (2014). Michez D, Eardley C (2007). Monographic revision of the bee genus Molecular phylogeny, biogeography, and host plant shifts in the Melitta Kirby 1802 (Hymenoptera: Apoidea: Melittidae). An bee genus Melitta (Hymenoptera: Anthophila). Mol Phylogenet Soc Entomol Fr 43: 379–440. Evol 70: 412–419. Michez D, Eardley C, Kuhlmann M, Patiny S (2007a). Revision of Eardley CD, Kuhlmann M (2006). Southern and East African Melitta the bee genus Capicola (Hymenoptera: Apoidea: Melittidae) Kirby (Apoidea: Melittidae). Afr Entomol 14: 293–305. distributed in the Southwest of Africa. Eur J Entomol 104: Eckert JE (1962). The relation of honey bees to safflower. Am Bee J 311–340. 102: 349–350. Michez D, Eardley CD, Kuhlmann M, Timmerman K, Patiny S Engel MS (2001). A monograph of the Baltic Amber bees and (2010). The bee genera Haplomelitta and Samba (Hymenoptera, evolution of the Apoidea (Hymenoptera). Bull Am Mus Nat Melittidae): phylogeny, biogeography and host–plants. Hist 259: 1–192. Invertebr Syst 24: 327–347. Engel MS (2005). Family-group names for bees (Hymenoptera: Michez D, Else GR, Roberts SPM (2007b). Biogeography, floral Apoidea). Am Mus Novit 3476: 1–33. choices and re-description of Promelitta alboclypeata (Friese 1900) (Hymenoptera, Apoidea, Melittidae). Afr Entomol 15: Free JB (1993). Insect Pollination of Crops. 2nd ed. London, UK: 197–203. Academic Press. Michez D, Kuhlmann M, Ivanov SP, Radchenko VG (2012). Description of four new species in the bee genus Melitta Kirby, 1802 (Hymenoptera: Melittidae). Zootaxa 3337: 57–67.

458 ÖZBEK / Turk J Zool

Michez D, Patiny S (2002). West-Palaearctic Dasypoda Latreille, 1802 Palmer-Jones T, Forster IW, Clinch PG (1966). Observations on the biogeography (Apoidea, Melittidae). Beitr Hymenopt-Tagung pollination of Montgomery red clover (Trifolium pratense L.). Stuttgart 48–50. New Zeal J Agr Res 9: 738–747. Michez D, Patiny S (2005). World revision of the oil-collecting Parker FD, Batra SWT, Tepedino VJ (1987). New pollinators for our bee genus Macropis Panzer 1809 (Hymenoptera: Apoidea: crops. Agr Zool Rev 2: 279–304. Melittidae) with a description of a new species from Laos. An Pedersen MW (1961). Lucerne pollination. Bee World 42: 145–149. Soc Entomol Fr 41:15–28. Pekkarinen AO, Berg I, Calabuig L, Janzon A, Luig J (2003). Michez D, Patiny S (2006). Review of the bee genus Eremaphanta Distribution and co-existence of the Macropis species and their Popov 1940 (Hymenoptera : Melittidae), with the description cleptoparasite Epeoloides coecutiens (Fabr.) in NW Europe of a new species. Zootaxa 1148: 47–68. (Hymenoptera: Apoidea, Melittidae and Apidae). Entomol Michez D, Patiny S, Danforth B (2009). Phylogeny of the bee family Fennica 14: 53–59. Melittidae (Hymenoptera: Anthophila) based on combined Quilis PM (1928). Estudio monográfico de las Dasypoda Latr. Eos 4: molecular and morphological data. Syst Entomol 34: 574–597. 173–241 (in Spanish). Michez D, Patiny S, Rasmont P, Timmermann K, Vereecken NJ Radchenko VG (1987). Nesting of Dasypoda braccata Eversm. (2008). Phylogeny and host-plant evolution in Melittidae s.l. (Hymenoptera: Melittidae) in the south-western Ukraine. (Hymenoptera: Apoidea). Apidologie 39: 146–162. Entomologicheskoe Obozrenie 67: 299–301 (in Russian with Michez D, Pauly A (2012). A new species of the Palaearctic genus English translation in Entomol Rev 75: 57–60). Dasypoda Latreille 1802 (Hymenoptera: Dasypodaidae) from Radchenko VG, Pesenko YA (1989). A key to the bees of the genus the Great Rift Valley in Ethiopia. Zootaxa 3181: 63–68. Dasypoda Latreille (Hymenoptera: Melittidae) of the European Michez D, Terzo M, Rasmont P (2004a). Révision des espèces ouest- part of the USSR. Trudy Zool Inst Akademii Nauk SSSR 188: palearctiques du genre Dasypoda Latreille 1802 (Hymenoptera, 114–121. Apoidea, Melittidae). Linz Biol Beitrage 36: 847–900 (in Rozen JG, Jacobson J (1980). Biology and immature stages of French). Macropis nuda, including comparisons to related bees. Am Michez D, Terzo M, Rasmont P (2004b). Phylogénie, biogéographie Mus Novit 2702: 1–11. et choix floraux des abeilles oligolectique du genreDasypoda Schletterer A (1890). Apidarum species novae descriptae. Entomol Latreille 1802. An Soc Entom Fr 40: 421–435 (in French). Nachrichten (Berlin) 16: 225–238. Nabhan GP, Buchmann SL (1997). Services provided by pollinators. Stage GI (1966). Biology and systematics of the American species of In: Daily G, editor. Nature’s Services: Societal Dependence on the genus Hesperapis Cockerell. PhD, University of California, Natural Ecosystems. Washington, DC, USA: Island Press, pp. Berkley, CA, USA. 133–150. Velthuis HHW, Doorn A (2006). A century of advances in bumblebee O’Toole C (1993). Diversity of native bees and agroecosystems, In: domestication and the economic and environmental aspects of LaSalle J, Gauld ID, editors. Hymenoptera and Biodiversity. its commercialization for pollination. Apidologie 37: 421–451. Wallingford, UK: CAB International, pp. 169–196. Warncke K (1973). Die westpaläarktische Arten der Bienen Familie O’Toole C, Raw A (1991). Bees of the World. London, UK: Blandford Melittidae (Hymenoptera). Polskie Pismo Entomol 43: 97–126 Publishing. (in German). Özbek H (1976). Pollinator bees on alfalfa in the Erzurum region of Waser NM, Ollerton J (2006). Plant-Pollinator Interactions: From Turkey. J Apicult Res 15: 145–148. Specialization to Generalization. Chicago, IL, USA: University Özbek H (1979). Erzurum civarında yonca (Medicago sativa of Chicago Press. L.) ve korunga (Onobrychis sativa L.)’daki polinatör arılar Whitehead VB, Steiner KE, Eardley CD (2008). Oil-collecting (Apoidea:Hym.) bunların faaliyetleri, meyve ve tohum bees mostly of the summer rainfall area of southern Africa bağlamaya etkileri. Erzurum, Turkey: Atatürk Üniversitesi Yay. (Hymenoptera: Melittidae: Rediviva). J Kansas Entomol Soc No. 516, Zir. Fak. Yay. No. 235, Araş. Ser. No. 152 (in Turkish). 81: 122–141. Özbek H (1980). Doğu Anadolu Bölgesi’nde Çayır Üçgülü (Trifolium Woodcock TS (2012). Pollination in the Agricultural Landscape. pratense L.)’nü tozlayan arılar (Hymenoptera: Apoidea). Temel Best Management Practices for Crop Pollination. Guelph, ON, Bil Derg Seri-A 4: 61–66 (in Turkish). Canada: Canadian Pollination Initiative, University of Guelph. Özbek H (2008). Türkiye’de yonca bitkisini ziyaret eden arı türleri ve Wu YR (1978). A study of Chinese Melittidae with description of Megachile rotundata F. (Hymenoptera: Megachilidae). Uludağ new species. Acta Entomol Sinica 21: 419–428. Arıcılık Derg 8: 17–29 (in Turkish). Özbek H (2011). Korunga (Onobrychis viciifolia Scop), önemli bir arı bitkisi. Uludağ Arıcılık Derg 11: 51–62 (in Turkish).

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