﻿The bee genus Anthidiellum in Vietnam: descriptions of five new species and the first male of Anthidiellumcoronum (Hymenoptera, Megachilidae)

﻿Abstract The Vietnamese fauna of bees in the Anthidiellum Cockerell (Megachilinae, Anthidiini) is reviewed. Seven species are recognized, representing two subgenera. Five new species are described and figured as: Anthidiellum (Clypanthidium) nahang Tran, Engel & Nguyen, sp. nov., A. (Pycnanthidium) ayun Tran, Engel & Nguyen, sp. nov., A. (P.) chumomray Tran, Engel & Nguyen, sp. nov., A. (P.) flavaxilla Tran, Engel & Nguyen, sp. nov., and A. (P.) cornu Tran, Engel & Nguyen, sp. nov. from the northern and central highlands of Vietnam. Two previously described species are newly recorded for the fauna: A. (P.) carinatum (Wu) and A. (P.) coronum (Wu), with the male of the latter species described and illustrated for the first time. An identification key is provided for all species of Anthidiellum occurring in Vietnam.


Introduction
The genus Anthidiellum Cockerell (Anthidiini) consists of typically small, robust, megachiliform to somewhat bombiform bees. It can be separated from other genera by the following characteristics: body small, robust, metasoma oval-rounded, with strongly developed omaular carinae/lamellae, and an often-lamellate pronotal lobe (Michener 2007). Species are frequently black, often with maculae laterally or with unbroken bands on the terga (see species of Ranthidiellum Pasteels: Engel 2009;Nalinrachatakan et al. 2021). Additionally, the juxtantennal carinae are absent; the subantennal sulci are outwardly arcuate; the axillae are rounded, without a spine; the mesoscuto-mesoscutellar sulcus is broad; the mesoscutellum lacks lateral spines, but typically extends posteriorly as a broad, thin, truncate, or medially emarginate lamella overhanging the metanotum and propodeum; behind the propodeal spiracle there is a fovea, delimited by a carina, although sometimes the fovea is no larger than the spiracle; the jugal lobe of the hind wing is less than one-half as long as the vannal lobe; cu-v in the hind wing is less than one-half as long as 2M+Cu; the arolia are well developed; the mandible of the female has three or four teeth (tri-or quadridentate), while the male has two or three teeth (bi-or tridentate) (Michener 2007).
Currently, the genus Anthidiellum comprises nearly 65 described species in seven subgenera, most of which are found in the Old World (Pasteels 1972;Michener and Griswold 1994;Griswold 2001;Wu 2004;Michener 2007;Engel 2009;Niu et al. 2016;Soh et al. 2016;Kumar et al. 2017;Nalinrachatakan et al. 2021). There are about 30 species known from Asia, and about half of the species occur in Southeast Asia, all of which belong to the subgenera Clypanthidium Pasteels, Pycnanthidium Krombein, and Ranthidiellum Pasteels. In Vietnam, only two prior records of the genus were known from northern provinces (Khuat et al. 2012). However, upon re-examination, the specimens of Khuat et al. (2012) are misidentified, one belonging to Heriades Spinola (Osmiini) and the material of the other now missing. Recently, five new species and two newly recorded species of Anthidiellum were discovered in the northern and central highlands of Vietnam. Herein, we describe the five new species, as well as the first male of Anthidiellum (Pycnanthidium) coronum (Wu, 2004). Illustrations and a key are also given to all species of the genus from Vietnam. Table 1 summarizes the species of Anthidiellum currently known from Vietnam, with information on the known sexes and distribution.

Materials and methods
Specimens examined in the present study are deposited in the collection of Hymenoptera of the Institute of Ecology and Biological Resources (IEBR), Hanoi, Vietnam and Division of Invertebrate Zoology, American Museum of Natural History, New York, USA (AMNH). Adult morphological and color characters were examined with a Nikon SMZ745 stereomicroscope, while images were photographed with a Nikon SMZ800N digital stereomicroscope, and with an attached ILCE-5000L/WAP2 digital camera. Stacked focus images were prepared using Helicon Focus 7. Lastly, all files were processed with Adobe Photoshop CS6. The morphological terminology used in the descriptions follows Engel (2001) and Michener (2007), with certain body metrics following those of Niu et al. (2004): body length: measured from the base of the antennal torulus to metasomal apex (in dorsal view), head length: measured from the medioapical margin of the clypeus to the upper margin of the vertex (in facial view), head width: measured at the widest point of the head across the compound eyes (in facial view), eye width: the greatest width of the compound eye (in profile), genal width: the greatest width of the gena (in profile), intertegular distance: measured between the inner rims of the tegulae (in dorsal view). The abbreviations F, S, and T (followed by Arabic numerals) refer to numbered flagellomeres, metasomal sterna, and metasomal terga, respectively. Additional abbreviations: NP, National Park; RS, Ranger Station. Diagnosis. The female of this species is most similar to that of A. (Clypanthidium) popovii (Wu, 1962), as both have the mandible much broader apically than basally; metatibia and metabasitarsus both without a longitudinal carina on the prolateral surface; metabasitarsus slender, width much less than greatest width of metatibia; forewing with veins bicolorous; and metasomal T1-T3 black. The new species can be distinguished from the female of the latter species by the following: mandible with interspace between the first two teeth broad, about 2× the interspace between the second and third tooth (mandible with interspace of the first two teeth narrow, subequal to that between the second and third tooth in A. popovii), mesoscutum with postero-lateral corner forming an obtuse angle (mesoscutum with postero-lateral corner forming a nearly right angle in A. popovii), clypeus with small yellow markings laterally (clypeus without yellow markings laterally in A. popovii), forewing rather transparent basally and dark brown distally (forewing dark basally and yellow distally in A. popovii), metasomal T4 black and T5-T6 yellow (metasomal T4-T5 yellow, T6 black in A. popovii).  Engel & Nguyen, sp. nov., holotype, female A lateral habitus B dorsal habitus C facial view D mesosoma in dorsal view E head and mesosoma in profile F apical metasomal terga G metapretarsus, red arrow indicating arolium. Scale bars: 1 mm (A-F); 0.5 mm (G).
Sculpturing and texture. Mandible with small, dense, nearly contiguous punctures. Clypeus with round, dense, nearly contiguous punctures of unequal sizes, puncture sizes larger laterally than those on disc (Fig. 1C). Supraclypeal area and paraocular area with round, dense, nearly contiguous punctures, puncture sizes larger and rougher than on clypeus. Vertex with large, coarse, dense, contiguous or nearly contiguous punctures. Mesoscutum with round, distinct, dense, nearly contiguous punctures; mesepisternum with punctures as on mesoscutum; mesoscutellum with punctures as on mesoscutum except some slightly larger and coarser (Fig. 1D, E). Metasomal T1-T4 with round, small, dense punctures, T5-T6 with wrinkled punctures.
♂: Latet. Etymology. The specific epithet is a toponym for the type locality, the Na Hang district in Tuyen Quang Province. The name is treated as a noun in apposition.

Subgenus Pycnanthidium Krombein, 1951
Based on the presence or absence of a longitudinal carina on the prolateral surface of the metatibia and metabasitarsus and the normal or enlarged metabasitarsus of the female, Pycnanthidium can be divided into two distinctive groups: the first group with nine species includes A. carinatum (Wu), A. biroi (Friese), A. forstenii (Ritsema), A. nigriceps (Friese), A. riparium (Cockerell), A. smithii (Ritsema), A. ayun Tran, Engel & Nguyen, sp. nov., A. chumomray Tran, Engel & Nguyen, sp. nov., and A. flavaxilla Tran, Engel & Nguyen, sp. nov., while the second group, with a similar number of species, includes A. butarsis Griswold, A. coronum (Wu), A. krombeini Griswold, A. latipes (Bingham), A. melanaspis Cockerell, A. ramakrishnae (Cockerell) Diagnosis. This female of this species is most similar to A. (P.) chumomray (vide infra), sharing with it the following characters: metatibia and metabasitarsus with a longitudinal carina on prolateral surfaces, and metasomal T2, supraclypeal area, pronotal lobe, and axillae black. It can be separated from that species easily by the following characters: mandible tridentate, teeth gradually longer and teeth sharp apically; clypeus approximately 1.4× as broad as long and with trapezoidal yellow marking medially; mesoscutellum convex and bigibbous; paraocular area black.
Sculpturing and texture. Outer surface of mandible with abundant, small, dense punctures except larger, wrinkled punctures on proximal half. Clypeus with dense, shallow punctures, puncture much smaller on apical margin than on disc. Paraocular area, supraclypeal area, and frons with large, coarse, contiguous punctures. Vertex with round, dense punctures of unequal sizes, puncture sizes smaller than those on frons. Mesoscutum with large, coarse, contiguous punctures; mesoscutellum with contiguous punctures of unequal sizes, puncture sizes smaller than those of mesoscutum (Fig. 2D). Metasomal T1-T6 with small, round, dense punctures except punctures larger laterally.
Color. Body black except as follows: clypeus with trapezoid yellow marking except lateral and apical margins black (Fig. 2C). Mesoscutum with short, thin yellow markings latero-anteriorly (Fig. 2D). Metasomal T1 with yellow markings laterally; T3 basally with yellow band and large interrupted medially; T4 basally with yellow band and narrow interrupted medially (near as continuously in some paratypes); T5 basally with yellow band ( Fig. 2A, B, F).
♂: Latet. Etymology. The specific epithet is a toponym for type locality, the Ayun commune in Gia Lai Province. The name is treated as a noun in apposition.    Remarks. This species can be separated from the similar species A. smithii (Ritsema) by the following combination of traits: punctures of mesoscutum mesad parapsidal line dense but not contiguous; axilla laterally not reaching tangent of lateral margin of mesoscutum; and clypeus more densely, finely punctate, and posterior margin of gena not as strongly carinate posteriorly.

Anthidiellum
Nesting biology. A nest was found in an unused wooden plank in a warehouse in Son La Province. The entrance hole of the nest was oval-shaped, with a length and a width of about 4 mm and 3 mm, respectively (Fig. 3G). A female was observed and collected when flying out from the nest. Diagnosis. The female of this species is most similar to A. ayun (vide supra). It can be separated from that species by the tridentate mandible and in which the teeth are subequal in length not sharply pointed; by the clypeus approximately 1.6× as broad as long and with a subhexagonal yellow mark medially; the flat mesoscutellum; and the paraocular area with yellow extending along the inner ocular margin to the lower antennal torular tangent.
Sculpturing and texture. Outer surface of mandible with small, wrinkled punctures. Clypeus with shallow, dense punctures, apical margin with puncture sizes much smaller than disc. Paraocular area and supraclypeal area with large, coarse, contiguous punctures (Fig. 5C). Frons and vertex with dense punctures of unequal sizes, puncture sizes smaller than those on clypeus. Mesoscutum with large, contiguous punctures, except polished and impunctate on vertical medio-apical margin; mesoscutellum with contiguous punctures, puncture sizes smaller than those on mesoscutum (Fig. 5B). Metasomal T1-T6 with small, round, dense punctures except punctures larger laterally.
Color. Body black except as follows: paraocular area with yellow extending from base to lower antennal torular tangent. Clypeus with subhexagonal yellow mark medially, apical margin black. Frons with small yellow spot (Fig. 5C). Gena with short yellow markings near upper posterior margin of compound eye (Fig. 5A). Mesoscutum with short, thin, transverse, yellow markings latero-anteriorly along anterior border (Fig. 5A, B). Profemur apically and prolateral surface of antero-vertical half of protibia with brownish yellow marking; mesotibia with small yellow marking basally and brown on prolateral surface of antero-vertical half. Metasomal T1 with yellow laterally; T3 with basal yellow band, with narrow interruption medially; T4-T5 basally with yellow bands; T6 with small yellow mark medially (Fig. 5A, B, E).
♂: Latet. Etymology. The specific epithet is a toponym for the type locality, Chu Mom Ray National Park in Kon Tum Province. The name is treated as a noun in apposition. Diagnosis. The female of this species is most similar to that of A. (P.) carinatum (Wu 1962) as both have the metatibia and metabasitarsus each with a longitudinal carina on the prolateral surface; tridentate mandibles, with the teeth sharp apically; similar yellow markings on the face; and metasomal T2 black. The new species can be distinguished in the female from the latter species by the following: mesoscutum with short anteriorfacing surface at medioapical margin, with anterior surface polished and impunctate (mesoscutum nearly straight medioapically, with dense punctures just before margin in A. carinatum); mesoscutellum black, strongly convex, with mediolongitudinal depression apically and giving apical surface a weakly bigibbous appearance (mesoscutellum nearly flat and yellow to yellowish brown on margin apicolaterally in A. carinatum).
Color. Body black except as follows: clypeus yellow except black on apical margin; supraclypeal area with yellow laterally bordering subantennal sulci; paraocular area with yellow marking extending along inner margin to about lower tangent of antennal toruli. Frons with small yellow drop above medially (Fig. 6C). Gena with yellow mark above near vertex and posterior to upper margin of compound eye (Fig. 6E). Pronotal lobe yellow except small, round, dull spot medially, mesoscutum with thin, transverse, yellow markings latero-anteriorly on anterior border; axilla yellow (Fig. 6A). Prolateral surface of protibia yellow to yellowish brown. Metasomal T1 with yellow markings laterally, T3 basally yellow except broadly interrupted medially, T4-T5 with basal yellow bands, T6 yellow medially (Fig. 6B).
♂: Latet. Etymology. The specific epithet is taken from the Latin adjective flāvus (meaning, "yellow") and the noun axilla (meaning, "armpit" or "side"), and refers to the notable yellow markings on the axillae. Paratype. Vietnam: 1♂, same data as holotype [IEBR]. Diagnosis. The male of this species is similar to that of A. (P.) coronum. The new species differs from that species by the generally dull integument (integument shinier in A. coronum); the form of the male gonostylus in which the mesal surface of mesal branch bears some long setae and the mesal branch is long with its lateral margins slightly convex, while the outer branch is shorter, slender, and nearly straight, and the apical margins of both branches are straight (the mesal branch is long, swollen, with lateral margins curved, the outer branch is shorter, slender, and nearly straight, and the apical margin of both branches is rounded in A. coronum).
Color. Body dull black except as follows: mandible yellow except brownish black apically; clypeus yellow except tawny yellow on apical margin; paraocular area with yellow extending along inner ocular margin to lower tangent of antennal toruli; supraclypeal area yellow apically and laterally; antennal space apico-ventrally with small, dull yellow-orange marking; gena with yellow markings posterior to upper border of compound eye, extending from near tangent with top of eye to exceeding tangent (Fig. 7A, C). Mesoscutellum with thin, dull yellow marking on apical margin and interrupted medially (Fig. 7B). Profemur apically with small yellow mark; prolateral surface of protibia with thin, yellow mark; mesotibia with small yellow mark basally; superior margin of prolateral surface of metatibia with thin, yellow mark; entire metabasitarsus yellow. Metasomal T3 with yellow band interrupted medially; T4 with yellow band (interrupted medially in paratype), T5-T6 with yellow, T7 with yellowish mark medially (T7 blackish in paratype) (Fig. 7B, E).
Pubescence. Outer surface and dorsal and apical margins of mandible with short, sparse, yellowish setae; ventral margin of mandible with short, yellowish setae intermixed with longer setae. Apical margin of clypeus with some short, yellowish setae; clypeus laterally, paraocular area, and basal half of supraclypeal area with some sparse, short, yellowish setae. Antennal scape with short yellowish setae; face above antennal torulus with tuft of long, yellowish, plumose setae. Vertex with sparse, short, yellowish setae. Mesoscutum and mesoscutellum with short, yellowish setae. Propodeum with dense, long, plumose, white setae. Prolateral surfaces of metabasitarsus and metatarsus with dense, erect, white setae; retrolateral surfaces of these same podites with tawny yellow setae. Metasomal S1 with short, white tuft of setae on apical margin; S2 with longer, white tuft of setae on apical margin; S3 with long, tawny yellow tuft of setae on medioapical margin; S4 with yellowish tuft of setae on apical margin; surface of S6 with long, yellowish setae, apical margin of S6 with long, yellowish, plumose setae.
Color. Body black except as follows: clypeus yellow except yellow brown transparent on apical margin; mandible yellow except brownish black on apically; paraocular area with yellow marking extending along the inner margin to above the antennal socket; supraclypeal area with yellow marking as Fig. 8C; antennal space apico-ventrally with small yellow marking; gena with yellow markings extending from the twothird of the eye to exceed the top of eye (Fig. 9C). Pronotal lobe yellow, except yellow transparent in apical margin and a yellow brown transparent spot on the median area; in dorsal view, mesoscutum lateral margin with thin, short, paint yellow markings (or absent in some specimens); tegula basally with yellow markings; mesoscutellum with  yellow marking and interrupted on apico-medially, apical margin of yellow to yellow to yellow transparent marking; axilla black (or with small, yellow spot in some specimens) (Fig. 9D). Profemur latero-apical with small yellow markings; outer surface of protibia and mesotibia with thin, yellow marking, posterior and apical margins of metatibia with yellow marking and presence of two small brown marks embedded on yellow marking apically; all basitarsus yellow, tarsi dull tawny yellow. Metasomal T1-T2 laterally with small yellow markings, T3 basally with yellow band and interrupted medially, T4-T5 basally with yellow bands, T6-T7 with yellow, except baso-laterally (Fig. 9A, B).
Pubescence. Clypeus with some short, yellowish setae on apical margin; paraocular area and supraclypeal area with some sparse, short, yellowish setae; scape with short yellowish setae; face above antennal torulus and frons with tufts of long, white, plumose setae (Fig. 9C); vertex with sparse, short, yellowish setae. Margins of mandible with short, yellowish setae intermixed with some longer setae. Mesoscutum and mesoscutellum with short yellowish setae. Propodeum with dense, long, plumose, white setae. Prolateral surfaces of metabasitarsus and metatarsus with dense, erect, white setae; retrolateral surfaces of these same podites with tawny yellow setae. Metasomal S3 medio-apical margin with tuft of long, tawny yellow setae; surface of S6 with long, yellowish setae and apical margin of S6 with long, yellowish, plumose setae.

Key to species of Anthidiellum from Vietnam
Characters for the key were extracted from the original descriptions of Wu (1962Wu ( , 2004

Discussion
Previously, two species of Anthidiellum were recorded from the northern provinces of Vietnam (Khuat et al. 2012). Khuat et al. (2012) identified their material as Anthidiellum rasorium (Smith, 1875) (Phu Tho Province, label "Apoi.0237") and Anthidiellum sp. (Bac Giang Province) (deposited in the collection of Hymenoptera of IEBR). We examined the material reported by Khuat et al. (2012) and the material of the former species is a specimen of Heriades while the material of the latter is now missing. Given these misidentifications, the genus Anthidiellum had not been formally documented from Vietnam until the present report, even though the genus must have occurred here based on all of the extralimital records that implied a distribution for the clade across northern Vietnam, at the least. It is nice to be able to formally demonstrate the occurrence of the genus within the country, based on a small diversity of species. Considering the habitats in which the species were encountered, all Vietnamese species of Pycnanthidium were found on small rocks or collected in ash piles from the burning of small logs. Furthermore, all of the localities were next to small streams (Fig. 11). It seems likely that the bees were looking for a source of mineral salts and water at the time they were captured. It is greatly hoped that future studies can explore the biology of these species, ideally locating nests and discovering immature stages, nest associates, and floral associations.