The cuckoo bees of the genus Epeolus Latreille, 1802 (Hymenoptera, Apidae) from the Middle East and North Africa with descriptions of two new species

Epeolus is one of the more species-rich genera of cuckoo bees globally. Seventeen species are known from Europe, and 23 species have been recorded from various countries in the Middle East and North Africa. Epeolus iranicus sp. nov. and E. priesneri sp. nov. are newly described in this study, and E. seraxensis Radoszkowski, 1893, stat. nov., previously a subspecies of E. transitorius Eversmann, 1852, is regarded as a valid species and a lectotype is designated. The first records of E. ibericus and E. intermedius from North Africa are given, and the distribution of E. fallax in North Africa is confirmed. This study compiles known distributional records of the species of this genus from the studied region and provides an overview of the known species richness in the studied countries. Based on available records, Turkey (14 species), Morocco (11) and Iran (9) host the highest numbers of species of Epeolus, whereas in four countries only a single species has been recorded, and the presence of this genus in seven countries has yet to be confirmed.


Introduction
Cuckoo bees form an ecological group with representatives in three families, Halictidae, Megachilidae, and Apidae, characterised by their cleptoparasitic lifestyle. Female cuckoo bees do not forage or build their own nests but instead lay eggs within the nests of host bee species (Batra 1984;Michener 2007;Westrich 2018). Most species of cuckoo bees belong to the family Apidae, in which the subfamily Nomadinae forms the most species-rich group in most of the world (Michener 2007;Bossert et al. 2019). Epeolus Latreille, 1802 represents one of the more speciose genera of cleptoparasitic Nomadinae in the old world (Bogusch and Hadrava 2018). The species are sexually monomorphic in general, smaller or middle-sized (4-10 mm in total body length), and robust with a slightly conical metasoma. Their integument colouration is largely black, although in some species parts of the body are largely red or reddish brown, and almost all species possess bands and spots of white or yellowish tomentum on various parts of the body (Onuferko 2017;Bogusch and Hadrava 2018;Westrich 2018;Onuferko et al. 2019). Bees of the genus Colletes Latreille, 1802 are the only known hosts of Epeolus, and most species of Epeolus have been associated with only one species of Colletes; only some usually common and widespread species intrude nests of more Colletes hosts (Onuferko 2017;Bogusch and Hadrava 2018).
The genus has been the focus of several taxonomic and evolutionary studies in recent years. Onuferko (2017Onuferko ( , 2018Onuferko ( , 2019 published several revisions of Epeolus in the New World, as well as a phylogenetic and biogeographic study of the whole genus  and several other brief surveys on the ecology and ethology of this genus. Eardley (1990) revised the species in sub-Saharan but not North Africa. Bogusch and Hadrava (2018) reviewed and provided a key to the European species, Bogusch (2018) described three new species from east parts of Turkey and listed all the species known from this country and Bogusch (2019) described a new species from India and listed the species known from this country. Before the present study, it was not known how many species and which species of Epeolus occur in the Middle East and North Africa, or how numerous and common they are in the countries in which they occur.
This study is a compilation of Epeolus records based on specimens deposited in museum collections in Europe, USA and Morocco, as well as specimens from private collections. Warncke's notes on the distribution of bees of the genus Epeolus are also included herein. This is the first overview of bees of this genus from the Middle East and North Africa except for the comprehensive study of bees of Morocco (Lhomme et al. 2020). The objective of the present study is to provide a checklist of the species in the region, which includes two new species and a subspecies elevated to species level.

Epeolus fasciatus Friese, 1895
Published records. Southern and Central Europe, but recent records are known only from France and Spain (Bogusch and Hadrava 2018). Pesenko (1974) reported this species also from Russia -Rostov Province. Recorded also from Turkey and the Middle East (Alfken 1935;Pesenko 1974;Bogusch 2018).
Published records. North Africa, Turkey, and Spain -Canary Islands. Specimens from the Canary Islands differ from the North African populations and represent probably a separate species (necessary to confirm by molecular studies) (Bogusch and Hadrava 2018). Bischoff (1930)
Differential diagnosis. This species is most similar to E. transitorius and E. seraxensis, and all three species are characterised by the presence of apical (as opposed to submedial) labral tubercles (Figs 1d and 3d) and yellowish to reddish antennal segments, especially F1 and F2 (Figs 1c and 3c). The body is reddish in colour except the frons, vertex and the middle part of mesoscutum in females and entire mesoscutum in males, which are black ( Fig. 1a and 1b). Epeolus iranicus differs from E. seraxensis as follows: E. iranicus has sparser tomentum on the body, which does not cover the entire clypeus, frons, and mesopleura, shorter F1, and broken bands on the metasomal terga. Additionally, the frons is densely punctate but with shiny interspaces. The shape of male pygidium is much narrower with no emargination in the middle and differs from that of E. seraxensis (Figs 1i and 3i). From E. transitorius, this species differs as follows: in E. iranicus most of body is brownish or reddish in colour (in E. transitorius it is mostly black), on most parts of body the punctation is sparser, and the metasomal terga and sterna are smooth and shiny.
Head. Length to width ratio = 1.3 (Fig. 1c). Mandible light reddish, mandibular apex and preapical tooth dark brown. Labrum light reddish, semi-transparent, shiny, coarsely and sparsely punctate, apically with pair of small teeth separated by medial shallow emargination, apex with prominent whitish hair, with sides convex (Fig. 1d). Clypeus reddish, matt and with very fine and dense punctation, interspaces smaller than puncture diameters. Clypeus entirely covered by whitish tomentum. Frons black with basal part from clypeus to antennal tubercles reddish, with dense whitish hair around antennal socket, and with well-developed and sharp frontal keel. Vertex black, with sparse punctures, interspaces shiny and slightly greater than puncture diameters. Antenna reddish with flagellomeres dorsally partly brownish. Flagellomeres slightly longer than wide (L/W ratio = 1.05-1.1), F2 longer than other flagellomeres (L/W ratio = 1.35) (Fig. 1c).
Mesosoma. Pronotum reddish-brown and entirely obscured by whitish tomentum. Mesoscutum reddish with wide black medial line and whitish tomentum laterally. Punctation coarse and dense, interspaces narrower than puncture diameters but shiny. Mesoscutellum reddish, round, densely and coarsely punctate, punctures twice as large as on mesoscutum, axillar tooth (free portion of axilla) long and acute but slightly shorter than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum (Fig. 1e). Propodeum brownish, very finely sculptured, matt, and laterally with whitish tomentum. Mesopleuron reddish, partly obscured with dense whitish tomentum, coarsely and densely punctate, with interspaces shiny and smaller than puncture diameters (but ill visible under the tomentum) (Fig. 1f ). Wings brownish with dark brown venation. Legs light reddish or orange, partly covered by whitish tomentum, only tarsal claws brown, tibial spurs on middle and hind legs yellow.
Metasoma. Metasoma entirely reddish. T1 finely and sparsely punctate, interspaces shiny and larger than puncture diameters. T1 with lateral spots of whitish tomentum at the base and near the apex, T2-T4 with apical bands of tomentum, which are broken in the middle. T2-T4 densely but finely punctate with shiny interspaces and ill-developed depressions. T5 shiny with very fine and dense punctation, whitish tomentum on sides, pseudopygidial area short, with silvery pubescence (Fig. 1g). T6 reddish with slightly curved apex, bearing wide reddish pygidial plate, with long yellowish hair. S2 finely and sparsely punctate; interspaces wider than puncture diameters. Other sterna more finely and densely punctate. S5 wide and straight (see from side) (Fig. 1h). Processes on sides of S6 normal, with short projections, reddish.
Head. Length to width ratio = 1.2. Mandible light reddish, mandibular apex and preapical tooth dark brown. Labrum similar to that of female. Clypeus reddish, matt and with very fine and dense punctation, interspaces smaller than puncture diameters. Clypeus entirely covered by whitish tomentum. Frons black with basal part from clypeus to antennal tubercles reddish, with dense whitish hair around antennal socket, and with well-developed and sharp frontal keel. Vertex black, with sparse punctures, interspaces shiny and slightly greater than puncture diameters. Antenna reddish with flagellomeres dorsally partly brownish. Flagellomeres slightly shorter than wide (L/W ratio = 0.9), F3 a little longer than other flagellomeres (L/W ratio = 1.05), F2 longer (L/W ratio = 1.3).
Mesosoma. Pronotum black and entirely obscured by whitish tomentum. Mesoscutum black and with whitish tomentum laterally. Punctation coarse and dense, interspaces narrower than puncture diameters but shiny. Mesoscutellum reddish, round, densely and coarsely punctate, punctures slightly larger than on the mesoscutum, axillar tooth (free portion of axilla) long and acute but slightly shorter than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum. Propodeum brownish, very finely sculptured, matt, and laterally with whitish tomentum. Mesopleuron reddish, partly obscured with dense whitish tomentum, coarsely and densely punctate, with interspaces shiny and smaller than puncture diameters (but ill visible under tomentum). Wings brownish with dark brown venation. Legs light reddish or orange, partly covered by whitish tomentum, only tarsal claws brown, tibial spurs on middle and hind legs yellow.
Metasoma. Metasoma entirely reddish. T1 finely and sparsely punctate, interspaces shiny and larger than puncture diameters. T1 with lateral spots of whitish tomentum at the base and near the apex, T2-T4 with apical bands of tomentum, which are broken in the middle. T2-T4 densely but finely punctate with shiny interspaces and ill-developed depressions. T5 shiny with very fine and dense punctation, whitish tomentum on sides, pseudopygidial area short, with silver pubescence. T6 reddish, bearing reddish pygidial plate, with long yellowish hair (Fig. 1i). S2-S3 finely punctate with interspaces larger than puncture diameter, with white tomentum on apex, S4-S5 with prominent thick yellowish hair on apex.
Etymology. All known specimens were collected in Iran: iranicus (-a, -um). Ecology. Host and floral associations are unknown. Distribution. Recently known only from two nearby localities in Iran and several specimens from other localities (however, not properly localised) from the same country. Bischoff, 1930 Published records. North Africa -Morocco, Algeria, and Turkey. It was recorded usually in mountains (High Atlas Mts.). The holotype from "Laussitz", which means the region on border between Germany and Poland looks very similar to the specimens from Morocco and probably was wrongly labelled (Bogusch and Hadrava 2018).  Differential diagnosis. This species is probably closely related to E. flavociliatus, with which it shares the following morphological features: very small labral tubercles positioned near the apex, flat and shiny labrum (Fig. 2d), complete apical bands on the metasomal terga and elongate axillar spines (Fig. 2a). Both males and females of E. priesneri can be easily identified by the yellow clypeus (Fig. 2c), which is unique among the species of Epeolus from North Africa and the Middle East. Epeolus priesneri can be separated from E. flavociliatus by the densely punctate mesoscutellum (in E. flavociliatus the mesoscutellum is sparsely punctate), from both E. subrufescens and E. aureovestitus, which are both sometimes similarly coloured (Fig. 2c), by the position and size of labral tubercles (which are larger and more submedial in position in E. aureovestitus and E. subrufescens), from E. subrufescens also by the shape of mesoscutellum, and from also E. aureovestitus by the uninterrupted metasomal bands (interrupted in E. aureovestitus).

Epeolus laevifrons
Description. Female. Body length: 7.5 mm (Fig. 2a). Head. Length to width ratio = 1.3. Mandible yellow, mandibular apex and preapical tooth dark brown (Fig. 2c). Labrum yellow, semitransparent, shiny, coarsely and sparsely punctate, subapically with pair of small teeth separated by medial shallow emargination, sides convex (Fig. 2d). Clypeus yellow, shiny and with very fine and dense punctation in the middle, interspaces smaller or similar as puncture diameter. Lateral parts of clypeus with punctation of similar size but very sparse with large interspaces. Face with yellow base at clypeus, then to interorbital tubercle black, with dense whitish hair around antennal socket, and with well-developed frontal keel. Vertex with fine and sparse punctures, interspaces shiny and greater than puncture diameters. Gena with a prominent, lamella-like preoccipital carina. Antenna reddish, only scape, pedicel and F1 completely yellow, last two flagellomeres with brownish colour partly. Flagellomeres slightly shorter than wide (L/W ratio = 0.9), F2 a little longer than other flagellomeres (L/W ratio = 1) (Fig. 2c).
Mesosoma. Pronotum reddish-brown and entirely obscured by yellowish tomentum. Mesoscutum black with yellowish tomentum, with dense punctation, interspaces narrower than puncture diameters. Mesoscutellum reddish, round, densely and coarsely punctate, punctures slightly larger than on the mesoscutum, axillar tooth (free portion of axilla) long and acute, slightly longer than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum (Fig. 2e). Propodeum black, very finely sculptured on the top, the rest shiny, and laterally with yellowish tomentum. Mesopleuron reddish, entirely obscured with dense yellowish tomentum, coarsely and densely punctate, with interspaces shiny and similar in size to puncture diameters (but ill visible under the tomentum) (Fig. 2f ). Wings brownish with dark brown venation. Legs light reddish or orange, tibial spurs on middle and hind legs yellow.
Metasoma. Metasoma entirely reddish. T1 finely and sparsely punctate, interspaces shiny and larger than puncture diameters. T1-T4 with entire bands of tomentum. T2-T4 densely but finely punctate with shiny interspaces and ill-developed depressions. T5 shiny with very fine and dense punctation, whitish tomentum on sides, pseudopygidial area short, with silver pubescence (Fig. 2f ). T6 reddish with slightly curved apex, bearing reddish pygidial plate, which is not very wide, with long brownish hair. S2 coarsely and densely punctate, interspaces narrower than puncture diameters or similar in width. Other sterna more finely and densely punctate. S5 wide and straight (see from side) (Fig. 2g). Processes on sides of S6 normal, with short projections, reddish.
Head. Length to width ratio = 1.27. Mandible yellow, mandibular apex and preapical tooth dark brown. Labrum similar to that of female. Clypeus yellow, shiny and with very fine and dense punctation in the middle, interspaces smaller or similar as puncture diameter. Lateral parts of clypeus with punctation of similar size but very sparse with large interspaces. Frons black, with dense whitish hair around antennal socket, and with well-developed frontal keel. Vertex with fine and sparse punctures, interspaces shiny and greater than puncture diameters. Antenna reddish, only scape, pedicel and F1 completely yellow, last four flagellomeres darker, brownish. Flagellomeres slightly shorter than wide (L/W ratio = 0.85), F2 longer than other flagellomeres (L/W ratio = 1.4).
Mesosoma. Pronotum black and entirely obscured by yellowish tomentum. Mesoscutum black with yellowish tomentum, with dense punctation, interspaces narrower than puncture diameters. Mesoscutellum reddish, round, densely and coarsely punctate, punctures slightly larger than on the mesoscutum, axillar tooth (free portion of axilla) long and acute, slightly longer than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum. Propodeum black, very finely sculptured and shiny in the middle, and laterally with yellowish tomentum. Mesopleuron black with reddish macula in the middle, entirely obscured with dense yellowish tomentum, coarsely and densely punctate, with interspaces shiny and similar in size to puncture diameters. Wings brownish with dark brown venation. Legs light reddish or orange, only coxae black, tibial spurs on middle and hind legs yellow.
Etymology. The species is named in dedication to Hermann Priesner , Austrian entomologist, specialist on Heteroptera and Thysanoptera, and the person who collected the holotype. The epithet priesneri is masculine and declined in the genitive case.
Ecology. Host and floral associations are unknown. Distribution. Only four specimens were found in collections, two from Morocco, one from Egypt and Chad (Tibesti Mts.). The species probably occurs in North Africa and in Sahara, distribution south of the Sahara and in the nearest countries in Asia and South Europe is likely but yet unconfirmed.
Published records. Southern and Central Europe, where the species is rare. Recorded also in the Middle East (Bogusch and Hadrava 2018). Known from Turkey, where it is locally numerous (Bogusch 2018  Differential diagnosis. This species is probably closely related to E. transitorius and E. iranicus, and all three species are characterised by the presence of apical (as opposed to submedial) labral tubercles (Fig. 3d) and yellowish to reddish antennal segments, especially F1 and F2 (Fig. 3c). The body is reddish in colour except the head and mesoscutum in both sexes, which are black. Epeolus seraxensis can be separated from E. iranicus by the denser tomentum on the body, which covers entire clypeus, frons, mesopleura and legs (Fig. 3a, b), and by the longer F1 (Figs 1c and 3c for comparison), and unbroken bands on the metasomal terga. The body construction in both sexes is more robust and similar to that of E. transitorius. The frons is densely punctate but with shiny interspaces (Fig. 3c). The male pygidium is wide and emarginated on the apical part, different from that of E. iranicus (Figs 1i and 3i). From E. transitorius, this species differs as follows: in E. seraxensis the metasomal bands are uninterrupted and most of body is brownish in colour and covered with whitish tomentum. The length of F1 in both sexes and shape of male pygidium support the treatment of E. seraxensis as a separate species. It is also close to Epeolus laticauda Bischoff, 1930 by dense tomentun on sterna, unbroken tergal bands, wide and bilobed pygidial plate (but in E. seraxensis wider and more distinctly bilobed). In E. laticauda labral tubercles are positioned very close to apex, not on the apical margin as in E. seraxensis.
Clypeus reddish, matt and with very fine and dense punctation, interspaces smaller than puncture diameters. Clypeus entirely covered by whitish tomentum. Face black with basal part from clypeus to antennal tubercles reddish, with dense whitish hair around antennal socket, and with well-developed and sharp frontal keel. Vertex black, with dense punctures, interspaces shiny and smaller than puncture diameters. Antenna reddish with flagellomeres dorsally partly brownish. Flagellomeres slightly longer than wide (L/W ratio = 1.2), F2 longer than other flagellomeres (L/W ratio = 1.7) (Fig. 3c). Mesosoma. Pronotum reddish-brown and entirely obscured by whitish tomentum. Mesoscutum black, reddish only laterally, with whitish tomentum laterally and white paramedian bands reaching from the base somewhere behind the middle part of mesoscutum. Punctation coarse and dense, interspaces narrower than puncture diameters but shiny. Mesoscutellum reddish, round, densely and coarsely punctate, punctures twice as larger as on mesoscutum, axillar tooth (free portion of axilla) long and acute but slightly shorter than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum (Fig. 3e). Propodeum reddish, very finely sculptured, matt, dorsally and laterally with whitish tomentum. Mesopleuron reddish, entirely obscured with dense whitish tomentum, coarsely and densely punctate, with interspaces shiny and smaller than puncture diameters (but ill visible under the tomentum) (Fig. 3f ). Wings brownish with dark brown venation. Legs light reddish or orange, on dorsal side entirely covered by whitish tomentum, only tarsal claws brown, tibial spurs on middle and hind legs yellow.
Head. Length to width ratio = 1.25. Mandible light reddish, mandibular apex and preapical tooth dark brown. Labrum similar to that of female. Clypeus reddish, matt and with very fine and dense punctation, interspaces smaller than puncture diameters. Clypeus entirely covered by whitish tomentum. Frons black with basal part from clypeus to antennal tubercles reddish, with dense whitish hair around antennal socket, and with well-developed and sharp frontal keel. Vertex black, with dense punctures, interspaces shiny and smaller than puncture diameters. Antenna reddish with flagellomeres dorsally partly brownish. Flagellomeres slightly shorter than wide (L/W ratio = 0.95), F2 longer than other flagellomeres (L/W ratio = 1.4).
Mesosoma. Pronotum reddish-brown with black line in the middle, and entirely obscured by whitish tomentum. Mesoscutum black, with whitish tomentum laterally and ill-developed white paramedian bands reaching from the base to the middle part of mesoscutum. Punctation coarse and dense, interspaces narrower than puncture diameters but shiny. Mesoscutellum reddish, round, densely and coarsely punctate, punctures twice as large as on mesoscutum, axillar tooth (free portion of axilla) long and acute but slightly shorter than mesoscutellum. Mesoscutellum with posterior margin extending over propodeum. Propodeum black, very finely sculptured, matt, dorsally and laterally with whitish tomentum. Mesopleuron black, entirely obscured with dense whitish tomentum, coarsely and densely punctate, with interspaces shiny and smaller than puncture diameters (but ill visible under the tomentum). Wings brownish with dark brown venation. Legs light reddish or orange, on dorsal side entirely covered by whitish tomentum, only tarsal claws brown, tibial spurs on middle and hind legs yellow.
Metasoma. Metasoma dark brown. T1 finely and sparsely punctate, interspaces shiny and larger than puncture diameters. T1 with whitish tomentum at the base and an unbroken apical band, T2 with C-shaped pattern of whitish tomentum on each side, apically connecting into an unbroken apical band. T3-T6 with unbroken apical bands of tomentum. T2-T5 densely but finely punctate with shiny interspaces and well-developed depressions. T7 reddish, bearing reddish wide and apically bilobed pygidial plate, with long brown hair on basal part (Fig. 3i). S2-S3 finely punctate with interspaces larger than puncture diameter, with white tomentum on apex, S4-S5 with prominent thick yellowish hair on apex.
Distribution. Turkmenistan (type location), in the Middle East currently reported from Iran and Israel.

Epeolus subrufescens Saunders, 1908
Synonyms (detailed in Bogusch and Hadrava (2018) landscape is covered by deserts (Saudi Arabia), or small countries (Bahrain, Kuwait). Second, the political situation in some countries makes impossible or exceedingly difficult to collect insects legally and safely, resulting in marked differences in the reported numbers of species between some neighbouring countries. Studied countries with the numbers of known species of Epeolus are shown in Fig. 4.
After three species described from Turkey (E. productuloides, E. turcicus and E. warnckei by Bogusch (2018) and one from Portugal and Spain (E. ibericus by Bogusch in Bogusch and Hadrava (2018)), two new species were described from the Middle East and North Africa in this study. First, E. iranicus was discovered in Iran and is in general appearance similar to E. transitorius. This species is certainly a new valid species and differs in more characters from the related E. seraxensis and E. transitorius. Four specimens of E. priesneri were discovered in two collections. This species is unique for the first sight with its completely red metasoma and yellow labrum and apex of clypeus. Regarding the distribution, it seems to occur inside and around Sahara. Last, E. seraxensis was put as a valid species, while it was described as a subspecies of E. transitorius. Its differences from E. transitorius and E. iranicus are large and thus it is necessary to regard E. seraxensis as a new species. However, the original description is incomplete and does not include photos or drawings of the specimens, the re-description of both sexes and photos of whole specimens and main characters are included in this study, as well as the lectotype is descignated.
Further studies on Epeolus of the Middle East and North Africa are needed to bring additional information on the distribution of the species and on the changes in their distribution. Several specimens in collections of OLML from eastern part of Turkey are probably representatives of species new to science but the differences from related species are minute and more material for further descriptions is needed. Last, most of Epeolus have unknown hosts, such as widely distributed species in Europe and/or the Middle East and North Africa (E. flavociliatus, E. transitorius). Finally, more information is needed about the ecology of the treated species (in terms of phenology and bee and floral host associations) to explain their distributions and identify which species are potentially more susciptible to habitat loss.