Review of the Epeolus cruciger species group (Hymenoptera, Apidae, Epeolus Latreille, 1802) of Asia, with the description of two new species

The six species of the Epeolus cruciger species group from Asia are reviewed. Two new species, Epeolus asiaticus Astafurova & Proshchalykin, sp. nov. (Mongolia, Russia) and E. gorodkovi Astafurova, sp. nov. (Tajikistan, Afghanistan) are described and illustrated. Epeolus alpinus Friese, 1893 is newly recorded from Kazakhstan; E. cruciger (Panzer, 1799) is newly recorded from Turkmenistan, Uzbekistan, and Kyrgyzstan; and E. mongolicus Astafurova & Proshchalykin, 2021 is newly recorded from Kyrgyzstan and Russia. An identification key for both sexes of all Asian members of this species group is presented.


Introduction
The present paper is part of a series of works dealing with the bees of the genus Epeolus Latreille, 1802 of the Asian Palaearctic (Astafurova and Proshchalykin 2021a, b, c). The genus Epeolus includes more 118 species spread across much of the globe; they occur throughout the Holarctic zone, from the west coast of the United States and eastwards to Europe and as far as Japan (Michener 2007  Pubescence coloration monochromatic (golden or copper); terga entirely covered with dense tomentum.  Thomson, 1872(nom. praeocc., nec Linnaeus, 1758: 212, ♀ (type locality: unknown), Zoological Museum, University of Lund, Sweden. Epeolus glacialis Alfken, 1913: 36, nomen novum for E. variegatus Thomson, 1872. Epeolus montanus Bischoff, 1930, ♀, ♂ (type locality: Warnemünde, Germany), Natural History Museum, Berlin. Epeolus pilosus Bischoff, 1930: 9-10, ♀, ♂ (type locality: Rositten [=Rybachij], Kaliningrad Prov., Russia), Natural History Museum, Berlin. Epeolus alpinus Bischoff, 1930(nom. praeocc., nec Friese, 1893: 9-10, ♀ (type locality: Saas, Switzerland), Natural History Museum, Berlin.  Astafurova and Proshchalykin (2021b: 14). Variability. Asian specimens examined are on average bigger than European ones (6.0-8.0 mm vs 5.0-6.0 mm). Female. Unlike E. cruciger and E. asiaticus sp. nov., this species does not have individuals with a red pattern on integunent of the metasomal terga. The pronotal lobe, mesoscutellum and axillae are red in most of studied Asian specimens; these structures are mostly black in specimens from the European range; only 6% of all examined females have a red labrum. Pubescence of the head and mesosoma, tergal bands or spots of tomentum are white or pale yellow. The mesoscutum is without tomentum in most specimens, rarely with weak tomentum anteriorly. Most examined specimens have widely interrupted apical bands of pale tomentum on T1 and T2 and two pairs of spots of pale tomentum on T3 and T4 (Fig. 5A), but sometimes the lateral spots on T3 and T4 are reduced and only a medial pair is present. Specimens examined from isolated populations of Sakhalin Isl. (Russia) differ from typical forms in having well-developed tomentum on the marginal zones of the terga, which are present as narrowly interrupted bands or even uninterrupted bands on T3 and T4 (Fig. 5B); the mesoscutum is denser punctate than in continental specimens. Male. The males do not show significant variability in coloration. Yellow-red coloration is absent, except on the mouth parts, legs (partly), tegulae and rarely the pygidial plate. Tergal bands of white tomentum are widely or narrow interrupted medially by regular brownish tomentum, sometimes reduced to two pairs of spots on T3 and T4; T1 apical bands can be rarely uninterrupted. Specimens from Sakhalin Isl. as well as females differ in having well-development apical bands of tomentum, which are present as uninterrupted bands on all terga or at least on T3 and T4. Further molecular studies might help to determine whether the forms from Sakhalin merit separate subspecies or species status.   Description. Female (holotype). Total body length 8.0 mm (Fig. 1A, B); forewing length (without tegula) 6.0 mm. Structure and sculpture: Head ( Fig. 2A) transverse, 1.26 times as wide as long. Labrum (Fig. 2E) 1.6 times as wide as long, rounded basally and later ally, apical margin slightly curved with small distinct medial tooth; sub-apically with two well-visible teeth; integument shiny, coarsely and densely punctate (15-30 μm / confluent-0.5). Clypeus densely and finely punctate (10-15 μm / confluent-0.5), narrowly impunctate along apical margin. Frons with developed frontal keel. Upper half of frons and ocellocular area with shiny interspaces between punctures (15-30 μm / confluent-1.5). Flagellomeres ca 1.1 times as long as wide. Mesoscutum coarsely punctate (25-40 μm / confluent-1.5), interspaces between punctures shiny and smooth; mesoscutellum areolate-punctate. Axilla short and flat, pointed apically, but without distinct tooth. Mesoscutellum with shallow medial longitudinal impression; poste rior margin scarcely extending over propodeum. Mesepisternum mostly areolate-punctate, with few interspaces ca one puncture diameter. Propodeal triangle shagreened; posterior vertical surface of propodeum shiny and smooth. Metasomal terga densely and finely punctate (10-15 μm / 0.5-1), interspaces shiny and smooth. Pseudopygidial area short, triangular. Pygidial plate trapezoidal, apically truncate. Processes on sides of S6 normal, with short projections. Sterna densely punc tured like terga (Fig. 2D). S5 wide, straight as seen in lateral view.
Pubescence: Pale tomentum yellow to white. Labrum with sparse thin golden setae. Paraocular and supraclypeal areas with dense tomentum obscuring integument, clypeus with sparse pubescence. Upper half of frons with long simple setae (Fig. 2C). Vertex with sparse thick (plumose) setae. Genal integument almost obscured by tomentum. Pronotum dorsally with tomentum obscuring integument. Mesoscutum with thick plumose setae, dense on anterior third and peripherally; with a few erect simple setae. Metanotal integument almost entirely obscured by tomentum. Mesepisternum with tomentum denser on upper half and laterally. Ventral parts of mesosoma with dense white tomentum. Legs with white setae. T1 with wide basal band of pale tomentum connected with apical band laterally; marginal zones on T1-T4 with uninterrupted bands of pale tomentum, but medially tomentum sparser and not obscuring integument. Setae on tergal discs brownish; sparser and shorter than on apical bands. Pseudopygidial area with silvery pubescence. Sterna with golden short and sparser setae; marginal zones of T2-T4 with white tomentum.
Male. Structure, sculpture, coloration and pubescence are similar to those of the female (Fig. 1C). Head (Fig. 2B) transverse, ca 1.2 times as wide as long. F1 1.2-1.4 times as wide as long, remaining flagellomeres about as long as wide or little longer. Pygidial plate (T7) shiny, coarsely and densely punctate, 1.1-1.2 times as long as basal width narrowed toward apex, with shallow punctures; apical margin slightly curved. Clypeus with dense tomentum obscuring integument. Marginal zones of S2 and S3 with dense uninterrupted white tomentum bands; S4 and S5 normal, with golden long setae. Gonostylus as on Fig. 9B, F. Variability. Female. Total body length is 4.5-9.0 mm. The mesoscutellum is usually flattened with a weak medial longitudinal impression, but in large specimens this impression can sometimes be deep. The labrum, mandible, pronotal lobe, tegulae, legs, axillae and mesoscutellum are always yellow-reddish (amber); the clypeus is usually yellow-reddish apically as well as scape and partly F1. The females of this new species exhibit considerable intraspecific variation in the metasomal coloration and degree of development of the tergal tomentum bands. This variability is expressed in a huge variety of combinations of these features (Fig. 7A-G). Among all the specimens examined, there is not one where such a combination was more or less the same. The coloration of terga on discs ranges from mostly black (but never wholly) to a well-developed yellowish pattern; the proportion of yellow differs, but yellowish coloration is common on pos- terior half T1 and T5 and as a narrow strip along marginal zones of T2-T4. The sterna are yellow-reddish on marginal zones and can be reddish, brownish or black on discs.
Apical bands on T1-T4 typically uninterrupted (Fig. 7E), but tomentum medially can be sparser and darker (Fig. 7C, D, F, G); or bands are distinctly interrupted (Fig. 7B). The tomentum coloration is yellowish, but varies from pale yellow to bright golden. The coloration of pubescence on tergal discs ranges from yellowish to brownish (i. e. can be contrasting or not with coloration of tomentum bands).
Male. Total body length 5.0-7.0 mm. The apical margin of the pygidial plate is sometimes straight or rarely slightly bilobed. The coloration of pedicel, scape and F1 varies from partly yellow-red to brownish. Variation in metasomal integument coloration is similar to that of the female with different proportions of black and yellow-red (Fig. 7H, I). Apical tomentum bands are typically uninterrupted (Fig. 7I), but sometimes tomentum setae medially are sparser and darker (Fig. 7H). Tergal discs setae are white, yellowish, golden or rarely brownish. The sterna can be brownish or black on discs, but typically it is with yellow-reddish pattern laterally and along marginal zones; marginal zones pale-yellow or yellow.
Etymology. The specific name "asiaticus" is an adjective in the nominative singular that means "Asian" in Latin and refers to the occurrence of this species in Asia.  Remarks. We also have examined 80 specimens of this species (36 ♀, 44 ♂) from the European part of Russia and from the Caucasus. We have not listed materials from Yakutia published by Davydova and Pesenko (2002). A few specimens were misidentified by these authors and belong to E. alpinus (vide supra). A record from Sakhalin (Proshchalykin et al. 2004) also corresponds to E. alpinus.
Variability. Female. Integument coloration. There are two main forms: dark with black/brownish metasoma (Fig. 6A, B) and light with reddish metasoma (Fig. 6C, D). Extremely dark specimens have yellow only on the mouth parts, tegulae and legs; this form is rare. A reddish labrum and mesoscutellum were found in most of the dark specimens examined. Extremely light individuals have a reddish or amber labrum, antennae, clypeus, lateral and lower part of mesosoma, mesoscutellum, axillae, metanotum, and mesosoma. In this case, the mesoscutum is partly reddish (laterally and with reddish spots posteriorly). Darker forms predominate in the forest zone and are rarer in the steppe zone. However, both forms can occur in the same location. Pubescence coloration. Pubescence of the head and mesosoma and tergal bands or spots of tomentum are white or pale yellow. Bright individuals (with yellow pubescence) are extremely rare and occur in the southern part of the range of this species. Coloration of tergal disc pubescence is quite variable and correlates with integument coloration: black or dark brownish in dark forms and light brownish (rarely yellowish) in light forms. Development of tomentum. The mesoscutum lacks tomentum or has only a pair of short paramedial strips. The development of white tomentum apical band or spots on terga is variable, but this tomentum is always interrupted medially. T1 and T2 have widely interrupted apical tomentum bands forming a pair of lateral spots, on T2 sometimes reduced to two pairs of small lateral spots (Fig. 6C). T3 and T4 are with two pairs of lateral spots or rarely with a single pair. Male. Males do not show significant variability. Yellow-red coloration is usually absent, except mouth parts, legs, tegulae and pygidial plate; labrum, pronotal lobe, mesoscutellum, axillae are only rarely reddish. Tomentum is white or pale-yellow.  ghanistan, Ghazni, Moqur, 2000m, 24.VI.1970.

Epeolus gorodkovi
Diagnosis. Structurally and in coloration, the new species is very similar to Epeolus alpinus but differs in having uninterrupted apical tergal bands, denser and lighter pubescence on tergal discs (light brown to yellowish) and yellowish marginal zones on terga (black or brownish in alpinus). The upper half of frons, ocellocular area and mesoscutum are mostly confluently punctate (with a few shiny interspaces) and similar to those in E. cruciger. Differences between the new species and other species of the cruciger group are outlined in Table 1.
Integument coloration. Head black, except partly red-yellowish mandibles, brownish antennae and apically yellowish F1. Mesosoma black, except red-yellowish tegulae, tibiae and tarsi. Metasomal terga black, but marginal zones pale-yellow to golden. Sterna brownish with marginal zones the same color as on terga.
Pubescence: Tomentum whitish to yellow (except sometimes brownish on tergal discs). Labrum apically with sparse thin setae. Paraocular and supraclypeal areas with dense tomentum obscuring integument, pubescence on clypeus sparser, shorter and shabby. Upper half of frons with long simple setae. Vertex with sparse thick (plumose) setae. Gena with dense tomentum, but not obscuring integument. Pronotum dorsally with tomentum obscuring integument. Mesoscutum with tomentum of adpressed plumose setae (dense on anterior third and peripherally) and long erect simple setae. Metanotal integumentalmost obscured by short tomentum. Mesepisternum and ventral parts of mesosoma with long tomentum obscuring integument. Legs with white setae. Terga (Fig. 4F) with uninterrupted apical (on marginal zone) light bands of tomentum; T1 entirely covered light tomentum, but with setae medially sparser and shorter; pubescence on other tergal discs short, relatively dense, the same color as on marginal zones or darker to brownish. Marginal zones of S2 and S3 with dense uninterrupted white bands of tomentum; S4 and S5 normal, with golden long setae. Gonostylus as in Fig. 9A, E.
Female. Structure, sculpture, coloration and pubescence are similar to those of the male (Fig. 3A, B). Head (Fig. 4B) 1.25 times as wide as long. Flagellomeres ca 1.1 as long as wide. Pseudopygidial area short, triangular. Pygidial plate trapezoidal, apically truncate. Processes on sides of S6 normal, with short projections. S5 wide, straight as seen in lateral view. Head with adpressed tomentum around antennal sockets (in the single female specimen). T1 with wide basal whitish band of tomentum medially separated by brownish sparser pubescence and connected with apical band laterally; brownish pubescence on tergal discs contrasting with light tomentum bands on marginal zones. Variability. The male specimen from Afghanistan has a red labrum, F1, pronotal lobes and pygidial plate.
Etymology. The new species is named in honor of famous Russian entomologist and zoogeographer Kirill B. Gorodkov (1932-2001, the collector of the type series.

Discussion
The Epeolus cruciger species group is distributed only in the Palaearctic region, and its range extends from northern Africa to the Russian Far East and China. Epeolus cruciger is most widespread and occurs from Europe over Central Asia to the Russian Far East. Epeolus alpinus is also widespread from Europe to the Far East, but it is mostly a boreal species and in the southern part of its range occurs in mountainous areas. Epeolus schummeli is a Western Palaearctic species, but is not known north of Poland. The rest of the species have narrow ranges or are endemic: Epeolus laevifrons (North Africa, Turkey), E. sigillatus (Greece: Crete), E. mongolicus and E. asiaticus (Mongolia and adjacent territory) and E. gorodkovi (mountains of Tajikistan and Afghanistan). No specimens of the group are recorded in Japan. The females of several species demonstrate considerable intraspecific variation, but the males are less variable. Two species-E. cruciger and E. asiaticus-exhibit extreme variation in metasomal integumental coloration, having dark and light forms. In E. cruciger, the black forms predominate in the forest zone and are rarer in the steppe zone. However, both forms can be found in the same location. The same rule works for pubescence coloration, as brighter pubescence is generally exhibited by individuals from the southern area of its range. The large variation in body size is characteristic of most of species of this group (difference up to 1.5-2 times between the smallest and largest specimens). It should be noted that E. alpinus specimens from Asia are on average bigger than European ones. The Sakhalin population of E. alpinus represents a great example of differences between isolated island populations and typical continental forms, expressed in the development of the apical tomentum on terga. However, this case needs further investigation to determine whether subspecies or species status is warranted. Remarkable vitiation is seen in the reduction of the second submarginal crossvein (incomplete or lacking completely) found in 5% of female specimens of E. asiaticus. A similar phenomenon was also found in species from North America (Scarpulla 2018), including E. americanus (Cresson, 1878) and E. asperatus Cockerell, 1909(Onuferko 2018.