Resin bees of genus Megachile, subgenera Callomegachile and Carinula (Hymenoptera, Megachilidae) from Thailand with description of a new species

Abstract Resin bees of the genus Megachile subgenus Callomegachile sensu lato (Hymenoptera; Megachilidae) from Thailand are reviewed. The 14 species treated include those described or revised in the subgenus Alocanthedon, a junior synonym of Callomegachile (three species), and in Carinula (one species). One new species is described, Megachile chiangmaiensis Chatthanabun and Warrit, sp. nov. The replacement name Megachile parornata Chatthanabun, Warrit and Ascher, nom. nov., is proposed for M. gigas Wu (not Schrottky), which is recorded for the first time outside China. For each species, maps and full label data for the examined material documenting occurrences in Thailand are provided. In addition, global ranges, floral associations, and other life history data are summarized and a key to the Thai species is provided for females.


introduction
Bees in the subgenus Callomegachile Michener, 1962, of the genus Megachile Latreille, 1802 (both sensu lato of Michener 2007) are resin and mud-collecting megachilines native to the Old World that vary from moderate in size to gigantic for a bee (9.0-40.0 mm) and have an elongate, parallel-sided "chalicodomiform" body shape. Callomegachile are widespread in the Old World where native to the Paleotropics including all of sub-Saharan Africa, most of Asia extending northwards to subtropical and temperate latitudes, and the Australian region. At least 115 described species of Callomegachile sensu lato are currently known (Ascher and Pickering 2020; including 8 species of subgenus Carinula Michener, McGinley & Danforth, 1994) making it the most species-rich subgenera of resin bees and the second most species-rich overall (after the leafcutter bees subgenus Eutricharaea Thomson, 1872) in the genus Megachile (the third most species rich bee genus with 1490 valid species globally; Ascher and Pickering 2020), Most Callomegachile species collect plant resins as material for nest construction, hence the common name resin bees. In common with other species of Michener's (2007) Megachile Group 2, species of Callomegachile do not fold regularlycut leaves to make their nests (a synapomorphy of his Group 1, corresponding to genus Megachile sensu stricto (Litman et al. 2011;Trunz et al. 2016;Gonzalez et al. 2019)), but some can incorporate irregularly-cut leaf pieces into nests, especially for making closures (Michener 2007).
In the New World, Megachile (Callomegachile) umbripennis Smith, 1853 is adventive on several Pacific Islands including the Hawaiian Islands and also locally in the Western Hemisphere (Michener 2007;Gonzalez and Engel 2012) where recently detected in South Florida . Megachile (Callomegachile) sculpturalis Smith, 1853 of East Asia is now adventive in Eastern North America and widely distributed, having been found in southern Canada and in all of the Eastern United States (and in the Central States as far west as Nebraska, Kansas, and Texas). In addition, Megachile (Callomegachile) rufipennis (Fabricius, 1793) and M. (Carinula) torrida Smith, 1853 are adventive in the West Indies.
As with the delimitation of Megachile sensu lato, there has been considerable variation in subgeneric classification of Callomegachile, with Michener (2000Michener ( , 2007 proposing a very inclusive concept of the group while noting the distinctiveness of several named lineages. However, other authors have partitioned these bees more narrowly, with Engel and Gonzalez (2011) describing a new subgenus Alocanthedon Engel & Gonzalez, 2011 based in part on clypeal shape in females and the presence of dense patch of black setae on male forewing. However, a recent molecular phylogenetic analysis (Trunz et al. 2016) treated Alocanthedon as a junior synonym of Callomegachile, which we follow here, pending more thorough investigation of relationships between the African and Asian taxa and, in particular, of the status of the gigantic Megachile such as M. pluto Smith, 1860 for which the name Eumegachilana Michener, 1965 is available (see Michener 2007).
In an analysis that resolved the traditional subgenus Callomegachile sensu lato (sensu Michener 2007) as polyphyletic, Trunz et al. (2016) found that Carinula, in-cluding the well-known Asian species M. stulta Bingham, 1897, were well separated from typical Callomegachile. For sake of completeness, we treat in this work all Thai resin bees including both M. (Carinula) and M. (Callomegachile) in the narrower sense, but with the former recognized as a separate subgenus in light of its divergent placement in Trunz et al.'s (2016) phylogenetic trees. It has distinctive characters such as a complete longitudinal median clypeal carina in females and lack of a front coxal spine in males (Michener 2007).
Morphological characters uniting Callomegachile sensu Michener (2007) include striate arrangement of punctures on mesoscutum and lower part of mesepisternum; mandibles of female bees usually equipped with 3 to 7 teeth with ridges that are minutely roughened (less so in Carinula, as noted by Michener 2007); small appressed hairs present on inner mandibular surface of adductor interspace. In males, the sixth metasomal tergum (T6) is weakly bilobed or lacks median emargination, and the gonoforcep is slender (broadened in Carinula) (Michener 1962(Michener , 1965(Michener , 2007. Although many Callomegachile species are relatively well known and easy to recognize as such, more taxonomic and phylogenetic work is needed to clarify both subgeneric and species limits and to document newly discovered species. Many species described historically have poor original descriptions, are highly variable morphologically (especially in hair color), and have been inaccurately or controversially classified. In addition, the Callomegachile sensu lato fauna of Southeast Asia, including Thailand, remains poorly documented, in spite of their abundance and general distribution across the region (Gonzalez and Engel 2012;Ascher et al. 2016). Furthermore, interpretation of their biogeography has been complicated by their propensity to become adventive both across oceans and, potentially, within Asia itself (see Ascher et al. 2016;Soh et al. 2016).
Here, we summarize the occurrence of Callomegachile sensu lato species in Thailand from (1) literature records (2) historical specimens in two of the largest insect collection facilities in Thailand (3) the National University of Singapore, Division of Biological Sciences, Insect Diversity Lab database and (4) specimens recently collected from numerous collecting trips from 2006-2019. Distributions records, maps of Thai distributions, floral records, measurements, and images of pinned vouchers are provided based on study of both historical and recently collected specimens. Image records available for six species on the citizen science portal iNaturalist were also reviewed. One Callomegachile species new to science is described along with two new records for Thailand, and a replacement name is proposed for a species described from China and newly detected in Thailand.

Materials and methods
Within Thailand, 304 Callomegachile specimens (169♀, 135♂) were examined, which were deposited at the Natural History Museum of Chulalongkorn University (NHM-CU-BSRU; 147♀, 130♂), Bangkok, the Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University (CMU; 5♀), Chiang Mai, the Department of National Parks, Wildlife and Plant Conservation (DNP; 4♀), Bang-kok, the Kasetsart Kamphaeng Saen Insect Collection (KKIC; 13♀, 5♂), Nakhon Pathom, Thailand. Additional specimens were examined in the Insect Diversity Lab Collection of the National University of Singapore including material on loan from the Oberösterreichisches Landesmuseum of Linz, Austria (curator Fritz Gusenleitner, including material assembled by Maximilian Schwarz). Type repositories used for comparison with specimens examined in this study are abbreviated as follows:

IZB
Chinese Types of the valid species-group taxa were examined to the extent possible, including those of some but not at all of the names in synonymy. Image records on the citizen science portal iNaturalist were reviewed and identified by JSA.
Specimens were examined and measured with a Zeiss Stemi 508 dissecting microscope equipped with an ocular micrometer or calipers. Body length was measured from edge of clypeus (in dorsal view) to apex of T6. Forewing length was measured from tegula to lateral wing margin. Interocellar distance (ID) and ocelloccipital distance (OD) were measured and these distances were calculated into ID/OD proportion. Male genitalia were dissected following a method modified from Gonzalez (2008). Photomicrographs were prepared using a Canon 7D Mark II digital camera attached to a T2-T2 1.6× SLR long-distance microscope lens, and were processed with Adobe Photoshop CS6. Measurements are reported in millimeters using Axiovision LE 4.8.2.0. Bees were placed in an insect relaxing jar for 3-4 days to soften the specimens for facilitating the examination of mandibles and labrums. Mandibular teeth are numbered sequentially starting from apex toward the base of the mandible. Morphological terminology follows that of Michener and Fraser (1978), Engel (2001), andMichener (2007).
Specimens from NHMCU-BSRU were collected during 1956-1971 (33♀, 4♂) mostly by Dr. Kloom Vajropala of NHMCU-BSRU and2006-2019 (112♀, 126♂) from recent surveys by the Thai authors. Label data including localities were recorded verbatim for each specimen and, following georeferencing if necessary, were used to construct distribution maps using Adobe Illustrator. Coordinates for the maps were generated based on specimen labels or, for records lacking GPS data, by georeferencing localities using Google Earth and GPS Geoplaner online. To obtain data on global distribution by country and primary subdivisions, literature records were critically reviewed from Tadauchi andTasen (2009), Ascher et al. (2016), and the Discover Life Bee Species Guide and World Checklist (Ascher and Pickering 2020), and new records obtained were validated for future inclusion in the latter source. Type localities and repositories are cited, with details provided for those species described from Thailand including new records.  Diagnosis. Female can be easily recognized by its large body size (18-22 mm); black body covered with black hairs throughout (Fig. 2a); clypeus without median tubercle; mandibles four teeth; apical margin of labrum truncate without tooth (Fig. 2d); mesoscutum with weak transverse wrinkle pattern on disc, posteriorly also with weakly transverse wrinkle pattern (Fig. 2e); yellow wings; black scopa. Male can be easily recognized by the presence of black setae patch on medial cell of forewings; apical of T6 with shallow concavity; front tibia modified (Engel and Gonzalez 2011).    Friese, 1911: 207. Chalicodoma (Callomegachile) disjuncta: Michener, 1965: 191. Diagnosis. Female can be recognized by its medium body size (13-18 mm); black body covered with black hairs throughout, except propodeal triangle and T1 with white hairs (Fig. 4a); apical margin of clypeus with two small tubercles (Fig. 4d); mandibles five teeth with two stout apical teeth at apex and three small teeth basally; labrum rectangle; apical margin of clypeus truncate with two lateral teeth (Fig. 4e); wings hyaline except fuscous apical part; black scopa (orange in part in females of the superficially similar leafcutter bee M. (Aethomegachile) conjuncta Smith, 1853 which also has a shorter and less parallel-sided metasoma, finer tergal punctures, and cutting edges on mandibles). Male is similar to female except paraocular area and apical margin of clypeus with white hairs (Fig. 5c); mandibles three teeth; labrum rectangle with round corners (Fig. 5d) Cameron 1907;Friese 1911;Cockerell 1912;Cockerell 1919;Flectcher 1920;Dover 1921;Schulthess-Rechberg 1935;Ascher et al. 2016 (Bingham 1897;Flectcher 1920;Dover 1921;Schulthess-Rechberg 1935); Reunion. (Pauly 2001;Ascher et al. 2016); Seychelles. Mahe, Morne Blanc, Praslin Island (Cameron 1907;Cockerell 1912;Pauly 2001;Ascher et al. 2016); Singapore.     Floral records. Throughout Thailand, M. (Callomegachile) disjuncta can be found abundantly in many agricultural plots that are planted with Crotalaria juncea L., a common plant species grown for providing essential nitrogen element to many crop plants in Thailand. Also, a common weed, Bidens pilosa L., is frequently visited by the species. One record of M. (Callomegachile) disjuncta was found on Cratoxylum cochinchinense (Lour.) Blume.

Genus
Comments. Female somewhat superficially resembles M. (Aethomegachile) conjuncta in size and overall appearance.  : Michener, 1965: 191. Diagnosis. Female can be recognized by its black medium body size (12-14 mm); vertex and pronotum covered with fulvous hairs; propodeal triangle and T1-T4 with tuft white hairs on lateral edges; apical margin of T5 with white hair band but interrupted at median (Fig. 7a); apical margin of clypeus with two small tubercles (Fig. 7c); mandibles five teeth with two stout apical teeth at apex and three small teeth basally; labrum rectangle with rounded corners (Fig. 7d); vertex with median carina (Fig. 7e); white scopa except black at apical area. Male is similar to female except mandible three teeth; labrum rectangular with shallow impression at median (Fig. 8d).

Megachile
Literature records. India. Khasia Hills (Cockerell 1911 erell 1911). An iNaturalist image shows four females among a group of bees photographed at Hin Tung, Mueang District, Nakhon Nayok Province (credit: scottyastro 2015).     Cockerell, 1922, from Canton (now Guangzhou in Guandong) in southern China is likely a junior synonym of M. faceta based on our examination of images of its type in the NMNH, whereas Wu (2006) placed it in the leafcutter subgenus Amegachile Friese, 1909. Multiple species of leafcutter bees present in the region including Thailand closely resembles M. facetula in color pattern, so all identifications must be considered structural characters as well.

Megachile (Callomegachile) fulvipennis Smith, 1879 Figs 9, 10
Megachile fulvipennis Smith, 1879: 68. Female holotype (NHMUK, examined) Nicobar Island, India. Megachile atratiformis sininsulae Cockerell, 1927: 160. Chalicodoma (Callomegachile) atratiforme sininsulae : Michener, 1965: 191. Chalicodoma (Callomegachile) fulvipennis: Michener, 1965: 191. (Engel, 2011) and M. (Callomegachile) odontophora (Engel, 2011), in overall appearance: black body covered with black hairs throughout; yellow wings; black scopa ( Fig. 10a, f) except smaller size (14-16 mm); punctures on mesoscutum and lower part of mesepisternum striated; mandibles five teeth with two stout apical teeth at apex and three small teeth basally; labrum rectangular (Fig. 10c).  thorax with white hairs except central area of mesoscutum and scutellum; metasomal terga covered with ferruginous hairs; scopa ferruginous except white basal area; apical margin of clypeus with one medioapical tubercle and two lateral tubercles (Fig. 12b, c); meso-and metatarsi with ferruginous hairs (Fig. 12a). These characters are used to associate male and female bees. Description. Female. Length. Total body length 14.28-15.90; wingspan 23.40-26.54; fore wing 10.01-11.34. Structure and color. Head black; paraocular area with dense black hairs; central area of clypeus with strong median carina; apical margin of clypeus with medioapical tubercle and two lateral tubercles; subtriangular supraclypeal area with sparse punctures, apical and median area with strong carina; mandible with two stout apical teeth at apex and three small teeth basally, without cutting edge; outer surface of mandible minutely roughened with long black hairs; labrum rectangular, with surface minutely roughened and brimmed with erected long brown hairs along margins, conspicuously at apex; gena with sparse punctures; almost bare vertex with sparse punctures, ID shorter than OD, ID/OD = 0.50 ± 0.01; antennae with ten flagella, first flagellomere wider than long but shorter than the second; body parallelsided, thorax covers with white hairs except central area of mesoscutum and scutellum; mesoscutum and lower part of mesepisternum with coarsely striate puncture pattern; procoxal base with conspicuous small carina, covered with sparse white hairs; pro-and mesotibiae with two spines at apices; metatarsus with one small spine at apex; protarsus covers with dense brown hairs; meso-and metatarsus cover with dense brown hairs on outer side, with dense ferruginous hairs inner side; wing brown with dark brown vein; T1 covers with sparse ferruginous hairs, with sparse punctures; T2-T5 cover with dense ferruginous hairs, dense punctures on pregradular area, sparse punctures on marginal zone; T6 covers with dense ferruginous hairs, with sparse punctures and round shape at apex; scopa ferruginous except the basal area with white.
Remarks. Known sites for this species are in the highlands.   -Waldo, 1914), in overall appearance and size: large body size (18-19 mm); black body covered with black hairs throughout; yellow wings. Female is easily distinguished by mesoscutum with distinctly transverse wrinkle pattern on disc, posteriorly also with well separated punctures (Engel and Gonzalez 2011). Male can be recognized by median cell of forewings without black setae patch; juxtamandibular flange present (Fig. 14d); basitarsi of pro legs with hook shape (Fig. 14e). Literature records. Malaysia. Kuala Lumpur, Pahang, Pangkor Island, Penang, Perak, Selangor (Engel and Gonzalez 2011 Remarks. This species was described from Peninsular Malaysia. It is remarkable that the first and only Thai specimen record is from Phayao Province in northern Thailand.   : Michener, 1965: 192. Diagnosis. Female can be recognized by its black large body size (20-26 mm); mesosoma and T1 covered with fulvous hairs (Fig. 16a); base of clypeus with large protruding tubercle (Fig. 16b); mandibles elongate with three teeth and small tubercle at base; labrum oblong with lateral impression (Fig. 16c); black scopa.   -Waldo, 1914) in overall appearance and size: large body size (20-24 mm); black body covered with black hairs throughout; mesoscutum with weak transverse wrinkle pattern on disc, also posteriorly with weakly transverse wrinkle pattern; yellow wings (except apical margin of clypeus with median tubercle (Fig. 18e); mandibles four teeth with three stout apical teeth at apex and small tooth basally; labrum oblong with pointed apical margin and two lateral teeth (Fig. 18d)). Male can be easily recognized by clypeus covered with densely long hairs; forewings with black setae patch on medial cell; modified front tarsi (Engel and Gonzalez 2011). Floral record. Engel and Gonzalez (2011) noted the species was captured on Sindora siamensis Teijsman & Miquel.

Megachile (Callomegachile) ornata Smith, 1853 Figs 19, 20
Megachile ornata Smith, 1853: 183; female syntype (NHMUK, examined) Indonesia. Megachile miniata Bingham, 1896: 199. Megachile ruficorbis Cockerell, 1927: 6. Diagnosis. Female can be recognized by its black large body size (17-19 mm); T1-T4 covered with black hairs; T2 with small patch of brick-red hairs laterally; T5-T6 covered with pale light yellow hairs (Fig. 20a); mandible three teeth (Fig. 20b); second spine of pro-and mesotibiae bifurcate (Fig. 20c); metatibiae with spine at apex (Fig. 20d); brick-red scopa.      supraclypeal area convex and subtriangular with rough surface and sparse punctures; mandible with three teeth, without cutting edge; outer surface of mandible minutely roughened with long brown hairs; labrum length twice as long as wide with round apex, surface minutely convex and rough with erect long brown hairs at apex; gena with sparse punctures; bare vertex with sparse punctures, ID shorter than OD, ID/OD = 0.28 ± 0.01; antennae with eleven flagella, first flagellomere wider than long, shorter than the second; body parallel-sided; scutum and scutellum hairless except anterior margin of scutum with brown hairs; lower part of metathorax with white hairs; scutum and lower part of mesepisternum with coarsely striate puncture pattern; procoxa covers with brown hairs; proand mesotibiae with two apical spines, mesotibial spine bifurcate; apex of metatibiae with spine at apex; pro-and mesotarsus with short brown hairs; metatarsus with dense short fulvous hairs inner side and short brown hairs outer side; forewing length yellow hyaline with yellowish-brown vein; T1 covers with black hairs; T2-T5 cover with brick-red hairs; T6 covers with pale yellow hairs, round apex; scopa fulvous-red.

Megachile
Comments. There are some suspect specimens that show variation in both sexes of M. umbripennis. One female collected from Phitsanulok province (BSRU AA-4620) shows the following variations: lack of fulvous hairs on disc area of mesoscutum and lack of white hairs on T2-T5 (Fig. 27a-h). Males collected from Chiang Mai province (BSRU AA-3654, BSRU AA-3662) and Suphan Buri province (KKIC-02) have fulvous hairs on T2-T5 instead of white hairs (Fig. 29a-k). Diagnosis. The species superficially resembles M. disjuncta (Fabricius, 1781) in terms of its overall appearance and size: white tuft of hairs on scutellum, propodeum, and first few segments of metasomal terga; however, the prominent apical half-circular impression of clypeus with strong median carina (Fig. 31e) differentiates M. chiangmaiensis sp. nov. from the former. Clypeal impression smooth with dense dark hairs at apex. Such a clypeal impression was also present in another species of Callomegachile, M. ramakrishnae (Cockerell, 1919), a rare bee collected in Tamil Nadu, India, although the impression in M. ramakrishnae is more or less shallower and the pattern of the mesosoma and white hairs band on T2-T3 are absent. The apex of the labrum is strongly pointed medially with two lateral teeth (Fig. 31f ).
Description. Female. Length. Total body length 12.57-13.64; wingspan 18.60-22.56; fore wing 9.66 Structure and color. Head black; paraocular area with dense black hairs; clypeus with prominent apical half-circular impression with strong median carina; clypeal impression smooth with dense dark hairs at apex; smooth area of subtriangular supraclypeal with sparse punctures; mandible stout and elongate with- out cutting edge, mandible with three apical teeth, outer surface minutely roughened with long brown hairs; surface of labrum minutely roughened, apex of labrum medially strongly pointed with two lateral teeth; gena with sparse punctures; sparse punctures on vertex with ID shorter than OD, ID/OD = 0.55 ± 0.06; antennae with ten flagella, first flagellomere wider than long and shorter than the second; body parallelsided; mesoscutum and lower part of mesepisternum with coarsely striate puncture pattern; mesoscutellum and propodeum with tuft of white hairs; procoxa with small ridge, covered with sparse brown hairs; pro-and mesotibiae with two spines at apices; apex of metatibiae truncate; pro-, meso-and metatarsi with dense brown short hairs; hyaline wings with smoky color at apex and dark brown veins; T1 and pregradular area of T2 covered with tuft of white hairs; T2-T5 with dense punctures on margin and short black hairs on each side; T6 covered with short black hairs, apex round shape; scopa black.
Etymology. The new species is named after the type locality. Remarks. Megachile chiangmaiensis sp. nov. can be found in the same province as the morphologically similar congeneric species, M. disjuncta, although the latter are abundantly collected throughout Thailand. The biology of M. chiangmaiensis is unknown.