Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species’ gene coalescents and morphology (Hymenoptera, Apidae) Author Williams, Paul H. Author Huang, Jiaxing Author Rasmont, Pierre Author An, Jiandong text Zootaxa 2016 4204 1 1 72 journal article 10.11646/zootaxa.4204.1.1 3f8866d2-529e-43ad-b971-29fc52a13858 1175-5326 192302 C050058A-774D-49C0-93F9-7A055B51C2A0 10. Bombus margreiteri Skorikov ( Figs 5, 6 , 19, 21 , 33 , 65 ) [ Bombus mendax Gerstaecker ; Morawitz 1880 :340 , in part;? Morawitz 1890 :352 ; misidentifications.] < Bombus mendax > subsp. altaicus Skorikov 1910b :329 (not of Eversmann 1846 :436, = B. melanurus Lepeletier ), type-locality citation (Cyrillic) ‘[ Altai (Sary-Tau)]’ . Lectotype queen by present designation ZISP examined, ‘ Altai , Sary-Tau’ ( Altai , Kazakhstan ). Note 1. Synonymised with B. margreiteri Skorikov (as B. mendax subsp. margreiteri Vogt ) by Williams (1991) , supported here. < Bombus mendax > subsp. margreiteri [ Vogt in] Skorikov 1910b :330, type-locality citation ( Cyrillic ) ‘[ Semirechensk province , Altai , Zabaykalsky province ]’ ( Zabaykalsky in 1910 = Transbaikal ). Lectotype queen by present designation ZISP examined, ‘Narynj, Turkestan’ (Tian Shan, Kyrgyzstan ). Note 2. Mendacibombus margreiteri (Skorikov [cited as Vogt]); Skorikov 1923 :149 ; Skorikov, 1931 :215 . Bombus ( Mendacibombus ) mendax subsp. altaicus Skorikov ; Bischoff 1930 :2 . [ Mendacibombus makarjini ( Skorikov); Skorikov, 1931 :fig. 18 male , misidentification.] Mendacibombus altaicus ( Skorikov); Skorikov, 1931 :215 . Bombus margreiteri Skorikov [cited as Vogt]; Peters & Panfilov 1968 :179 . [ Bombus ( Mendacibombus ) defector Skorikov ; P.H. Williams, 1991 : 42 in part; P.H. Williams 1998 : 99 in part; Ito & Kuranishi 2000 :286 ; Kawakita et al. 2003 :90 ; Cameron et al. 2007 :165 ; misidentifications.] Bombus altaicus Skorikov ; Yefremova 2001 :272 . Bombus (Mendacibombus) altaicus Skorikov ; Proshchalykin & Kupianskaya 2005 :23 ; Proshchalykin & Kupianskaya 2009 :64 . Note 1 ( altaicus ). There is no evidence from the original publication for the number of specimens regarded as types of the taxon altaicus by Skorikov. Although only a single type locality (region) is given in the original description, more than one syntype may have existed. Skorikov’s original description of the taxon altaicus cites the type locality as Altai ( Sary Tau ). The ZISP collection studied by Skorikov contains a queen that agrees with the original description and carries the labels: (1) gold disc; (2) white, printed ( Cryrillic ) ‘[k. F Moravitsa ]’; (3) white, handwritten ‘ mendax / Gerst. [female].’; (4) white, hand-written ‘ Mont . Altai . / Sary-Tau / 9400’. Schwarz .’; (5) red, handwritten ‘ Holotypus Bombus / mendax subsp. / altaicus Skor. [female, overwritten with male]’; (6) green, printed ‘ Mendacibombus / MD# 739 det. PHW’; (7) red, printed ‘ LECTOTYPE [female] / Bombus mendax ssp. / altaicus / Skorikov , 1910 / det. PH Williams 2012’; (8) white, printed ‘[female] Bombus / ( Mendacibombus ) / margreiteri / det . PH Williams 2012’. This specimen, which is complete, is regarded as one of Skorikov’s syntypes and is designated here as the lectotype in order to reduce uncertainty in the identity and application of the name. Note 2 ( margreiteri ). The name margreiteri was first published by Skorikov (1910a) , who described the taxon in a key couplet followed by ‘subsp. margreiteri Vogt’. Later Skorikov (1931) referred to the name as ‘ Mendacibombus margreiteri (O. Vogt, in litt.)’ [sic]. Therefore Vogt may have recognised the taxon as undescribed and may have supplied the name margreiteri . However, there is no evidence from Skorikov’s original publication that Vogt satisfied the other minimum criterion for availability ( ICZN, 1999: Article 12.1 ), including that Vogt supplied a description or diagnosis. Therefore the author of the nomenclatural act is deemed to be Skorikov ( ICZN, 1999: Article 50.1.1 ), not Vogt. Skorikov’s original description of the taxon margreiteri cites the type localities as Semirechensk province , Altai , and Zabaykalsky (Transbaikal) province , so multiple syntypes are expected to exist. The ZISP collection studied by Skorikov contains a queen that agrees with the original description and carries the labels: (1) black disc; (2) white, handwritten probably by Vogt ‘ mendax / margreiteri O.V. / Cotype. / Narynj. VI.08. / Turkestan. ’; (3) red, handwritten and crossed out with a large X ‘ Syntypus Bombus / mendax subsp. / margreiteri / Vogt [female]’; (4) green, printed ‘ Mendacibombus / MD# 738 det. PHW’; (5) red, printed ‘ LECTOTYPE [female] / Bombus mendax ssp. / margreiteri / Skorikov , 1910 / det. PH Williams 2012’; (6) white, printed ‘[female] Bombus / ( Mendacibombus ) / margreiteri / det . PH Williams 2012’. This specimen, which lacks most of the left flagellum, the left hindwing, and the last three joints of the right hindleg tarsus, is regarded as one of Skorikov’s syntypes sent to him by Vogt. Unfortunately, the location of the type locality ‘Narynj’ (= Naryn) is uncertain. From gazetteers, we have identified 32 geographical features associated with the name Naryn in the region of the former Turkestan. In Turkish, the adjective ‘narin’ translates as thin, slender, or slight, so it may have been applied frequently to narrow features in this region. A clue to the location of the type-locality Naryn may come from many specimens in the RMNH collection (which includes most of the Vogt collection) that are labelled ‘Narynj / Siebenstrom’ from 1908 in the same handwriting (e.g. B. turkestanicus : MD#3513‒3516). This is an association of names that was repeated in print by Vogt (1911) : ‘der Umgebung der Festung Narynj im Siebenstromgebiet und dem Boro-Chorogebirge’ (p. 51) as well as ‘aus der Festungswerks Narynj und dem Boro-Chorogebirge im Siebenstromgebiet’ (p. 58). This appears to place the ‘Narynj’ on these labels in what was in 1908 the northeastern province of Turkestan, Semirechye Oblast (or in German, Siebenstrom, both derived from the Kazakh ‘Zhetysu’, referring to the seven rivers: Ili, Qaratal, Bien, Aksu , Lepsy, Baskan, and Sarkand). Semirechye had been given as one of the type localities in the original description. According to Vogt’s biographer, de Boer (2004) , Vogt purchased these specimens from an insect dealer, Osip Emeljanovich Neshivov ( 1859‒1919 ), who lived ‘in Naryn, Tashkent’ (an earlier reference in de Boer, 2002 , to ‘Naryn, Dzharkent’ was incorrect: de Boer, in litt.) and who gave his address as Fortress Naryn. According to maps for the period 1899‒1916 , the province of Semirechye (Siebenstrom) then included an area to the south of lake Ysyk-Köl, to encompass the well-known modern (long, narrow) town of Naryn on the Naryn River, now part of central Kyrgyzstan . A. de Boer (in litt.) believes that this is where the collector Neshivov lived, although he also believes that other collecting sites like ‘Schlucht Burchan’ (Burchan gorge) may have been nearby (on the Burkan river upstream to the east) rather than in the Borohoroshan (as implied by Vogt handwritten labels, e.g. ‘Boro- Chorogeb. / Burchan. 8.09’, MD#1236), and that perhaps Neshivov mistook the location of the Borohoroshan (not a view shared here). Within this Kyrgyz Naryn there are earthworks with possible corner emplacements surrounding a compound ( 41.431546°N 76.016929°E ). Even more convincingly, there are earthworks that might represent a town wall or enclosure ( 41.434177°N 75.997418°E ) and which could be the fortifications (Festungswerks) mentioned by Neshivov and Vogt. However, Siebenstrom is often shown on maps from other periods as a narrower region or governorate to the north of the Tian Shan mountains which excluded the Naryn in modern Kyrgyzstan . If we were to assume that Siebenstrom implied somewhere in modern Kazakhstan and if we assume that within this region Mendacibombus species are unlikely to occur at elevations below 1000 m (and there are three species of Mendacibombus in the Vogt collection labelled Naryn), then from our search of the gazetteers we would have just two candidate areas left: Narynkol ( 42.725864°N 80.178319°E ) to the south of Siebenstrom in the narrow sense; and Naryn Zhotasy ( 49.004339°N 84.500323°E ) to the north of Siebenstrom. Vogt (1911) gives the impression that he included both Naryn and the Boro-Choro mountains (Borohoroshan) within the region of Siebenstrom. A. de Boer (in litt.) reports a Burchan gorge (in Borohoroshan) label with an addition ‘Naryntal’ (Naryn valley), which if it referred to the same Naryn, might imply proximity of Naryn to the Borohoroshan. C. Burgess (in litt.) has located another Naryn river, which is closer to both the centre of Siebenstrom and to the possible Neshivov collection site of Burchan gorge in the Borohoroshan. There are ruins near this river Naryn that could be another candidate for Vogt’s Naryn fortifications ( 44.440116°N 80.106918°E ). Nevertheless, until further information is available, for the present we follow de Boer in accepting that the Naryn on the specimen labels refers to the Kyrgyz town where Neshivov lived. Unlike de Boer, we accept that Vogt’s Burchan gorge is in the Borohoroshan (near 44.70342°N 79.82960°E ). The queen in the ZISP collection described above is regarded as a syntype of B. mendax subsp. margreiteri Skorikov and is designated here as the lectotype in order to reduce uncertainty in the identity and application of the name. Etymology. The species is named after M. Margreiter, who around 1910 was a schoolteacher in Vienna , who sold or sent many Austrian bumblebees to Vogt (de Boer, in litt.). Vogt sent the type material of this species (not collected by Margreiter), and probably the manuscript name margreiteri , to Skorikov. Taxonomy and variation. The interpretation of this species is based here on evidence from DNA, as well as on the form of the female labrum and of the male genitalia. This disagrees with earlier concepts ( Skorikov, 1931 ), diagnosed originally in terms of the hair colour pattern ( Skorikov, 1910b ), because the species appears to be much more variable in colour than was originally understood. Skorikov (1910b) described females of the taxon margreiteri s. str. from the Tian Shan (and Altai and Transbaikal, including MD#738) mountains as having the corbicula framed with rusty hairs, with the pale bands yellow and the hair on the lower side of the thorax and on the ventral side of the body black. Our COI tree shows that specimens of the taxon margreiteri s. str. and other specimens with a closely similar colour pattern (corbicula framed with rusty hairs, with the lower side of the thorax and the ventral side of the body black), but with the pale bands white or very slightly yellow (Skorikov’s taxon altaicus from the Altai , MD#739), have very short branch lengths between them ( Fig. 13 : the yellow-banded taxon margreiteri s. str . MD#319 and the white-banded taxon altaicus MD#329). Some females, especially workers from Mongolia and the Tian Shan (white-banded), have most of the hair on the outer side and edges of the hind tibia orange, except at the extreme proximal end where it remains black (MD#287, 288, 307, 327). A few females from Mongolia and the Tian Shan (white-banded) have more pale hair, both on the lower side of the thorax extending to the base of the midleg (some black hair intermixed), on all three femora, and on the ventral side of the metasoma (most extreme for the ‘semipale’ worker MD#287 and for the queens MD#4103, 4104). All of these individuals are interpreted as conspecific, as parts of the species B. margreiteri s. l .. There appears to be a disjunction between the northern Altai-Transbaikal population and the Tian Shan population. No specimens from this Tian Shan population (e.g. MD#4103, 4104) have been sequenced successfully. The disjunct population in Kamchatka ( Bischoff 1930 ; Ito & Kuranishi 2000 ) is remarkable for its wide separation from the Central Asian and Baikalian population by more than 3570 km (only slightly less if Skorikov’s [1910b] record for Transbaikal, given as Troitzkosavsk [= Kyakhta] in Skorikov, 1931 , is included) in combination with so little divergence in COI sequences ( Fig. 13 : no base-pair differences are uniquely shared by the Kamchatka samples MD#1265, 1268, compared with the Altai taxon margreiteri s. str . MD#319). These Kamchatka specimens are considered conspecific with B. margreiteri . In another surprising and large extension of the range, a taxon with much more extensively yellow-banded hair (and less black) is recorded here perhaps for the first time (but see Morawitz 1890 :352 for a possible record). The yellow hair extends onto the lower side of the thorax and onto the ventral side of the metasoma, with the corbicula orange-fringed. It was collected at only two neighbouring sites (at Heishi and Qushiang, near Dulan, in Qinghai, China) that are distantly disjunct and separated by more than 1270 km from the nearest other recorded site for the species, in Mongolia. These two Qinghai sites are in the mountains at the southeastern end of the Qaidam depression, in a northern extension of the Burhan Budai Shan. All specimens from Dulan sequenced for COI (4/55 specimens) share the same haplotype, which differs from all other B. margreiteri haplotypes only at position 271 (T substituted for C) and these samples are interpreted as conspecific with B. margreiteri ( Fig. 13 : the extensively yellow samples from near Dulan labelled ‘pale’ MD#289, 292, 293, 294 compared with the taxon margreiteri s. str . MD#319). The male genitalia do not differ appreciably. We do not name this population formally (as a subspecies) because we wish to avoid adding to the many unnecessary formal names for bumblebees below the rank of species. Throughout its range, except in Qinghai , the species B. margreiteri s. l. shows a dimorphism in the pale bands, with white-banded individuals (taxon altaicus ) and yellow-banded individuals (taxon margreiteri s. str. ) both recorded from Kamchatka , the Altai , and the Tian Shan ( Fig. 13 ). This dimorphism may be similar to that shown by B. handlirschianus in Western Asia (see the comments on B. handlirschianus ). However, for B. margreiteri s. l. , white-banded individuals are more frequent in Mongolia and yellow-banded individuals are more frequent in the Tian Shan and in Qinghai . Contrary to a previous interpretation of morphology ( Williams, 1991 ) when not all of the types could be examined, COI sequences from specimens identified from their yellow-banded colour pattern and black-fringed corbicula as Skorikov’s taxon defector are now found to be a separate species ( Figs 11‒12 ; see the comments on B. defector ). Diagnostic description. Wings nearly clear. Female hair colour pattern : generally black, but with pale hair (yellow or grey-white) in a large patch ventral to the base of the antenna, in a small patch or absent from the vertex of the head, in a transverse band anteriorly on the thoracic dorsum and extending laterally and ventrally to half way down the side of the thorax, or more rarely to the midleg base, in a transverse band posteriorly on the thoracic dorsum (scutellum; so the thoracic dorsum between the wing bases has the hair black, only rarely with pale hair intermixed laterally, adjacent and mesad to the tegula), on T1‒2, although T2 is pale with only a few black hairs intermixed along the posterior margin, orange hair sometimes on T3 as a posterior fringe and always on T4‒6, except T6 medially intermixed with short black hairs, hair of the ventral side of the metasoma usually black but sometimes pale. Hindleg tibia with the corbicular fringes often appearing double ( cf. B. defector , B. turkestanicus ): hairs on the corbicular surface and in the adjacent inner fringes usually extensively orange, but exterior to this in the outer fringes (anteriorly and posteriorly) black, or rarely with more black hairs in the inner fringes, although usually the inner fringes retaining many extensively orange hairs ( Fig. 22 ). Female morphology : labrum with the basal depression narrow, the transverse ridge broader medially than the basal depression, in the median third high, consistently convex throughout and not subsiding or interrupted, with only a few scattered medium or large punctures (slightly more for individuals from Kamchatka ), lateral tubercles smooth with few punctures ( Fig. 19 ) ( cf. B. defector , B. turkestanicus ). Clypeus in its central half with few widely spaced small punctures, fewer large punctures ( cf. B. defector , B. turkestanicus ). Hindleg tibia distal edge with broad spines (rastellum) often continuing just onto the posterior edge by two or three spines ( cf. B. defector , B. turkestanicus ). Male morphology : genitalia ( Fig. 33 ) with the volsella distally rounded (finger-shaped) and curled back dorsally but not anteriorly; volsella at its broadest near the midpoint of its length, the dorsal surface just distal to this point without a raised curved ridge just inside the inner margin. Gonostylus distally thick, rounded in section, and finger-like; gonostylus with the inner distal corner narrowly acute from both the inner and the dorsal aspects; gonostylus proximal half with the sides diverging ( Altai , Qinghai ). Penis-valve inner shoulder located at Ĺ 0.5× the length of the penis valve from the distal end to the broadest point of the spatha; penis valve proximal to the outer shoulder> 2× as broad as the penis-valve head; penis-valve head laterally compressed. Material examined. 56 queens 88 workers 33 males , from China , Kazakhstan , Kyrgyzstan , Mongolia , and Russia ( Fig. 65 : HUS , IAR , ISEAN , IZB , LP, MNHU , NHM , NME , OLL , PW, RMNH , UMONS , ZISP , ZMMU ), with 19 specimens sequenced (interpretable sequences listed in Figs. 11–13 ). Habitat and distribution. Flower-rich alpine and subalpine grassland, at elevations 164‒(2538)‒ 3526 m a.s.l.. A species with an unusual distribution among four distantly disjunct centres: (1) the central Tian Shan; (2) the Altai , Sayan, Mongolia and Buryatia mountains; (3) the Burhan Budai Shan; and (4) southern Kamchatka . Other genes should be checked to confirm that these are disjunctions within a single species. Individuals from Buryatia (Mondy: D. Michez, pers. comm.) and from the Burhan Budai Shan are from meadows at the upper elevational limit of trees, although there are few trees in the latter area. The population in Kamchatka is restricted to a small area where it may be associated with geothermal features (see below). This species overlaps with B. turkestanicus and B. defector in the Tian Shan, and it sometimes occurs together with one or (rarely) both of them. The modern Kamchatka population appears now to be a relic in the warmer south-eastern coastal areas of the peninsula, where the climate is warmed by the effect of the summer southerly storms ( Anonymous 2001; Newell 20 04 ). There is another more intriguing possibility—that the Kamchatka climate is also buffered locally by strong geothermal effects. Ebmer (1996) records that the bee Halictus rubicundus (Christ) is a widespread holarctic species with a small northern pocket of occurrence in the same region of south-eastern Kamchatka (Kronotsky), where all of the H. rubicundus specimens collected (by M. Krappe, in litt . to Ebmer) were confined to geothermally influenced sites. Similar close association of nests of the bee Lasioglossum nupricola Sakagami with geothermal features has been reported from two sites on Hokkaido , Japan , where this species has been interpreted as a climate relic ( Sakagami 1988 ). Food plants. ( Scrophulariaceae ) pink Pedicularis sp. (PW: the same species as shown in Figs 5‒6 , 31 .viii.2010 , Heishi near Dulan , Qinghai , China ). Behaviour. Mate-searching males perch on the tops of e.g. flowering spikes of Pedicularis sp. and from these pursue other bees that fly past before the males return to the same perch (PW: Figs 5‒6 , 31 .viii.2010 , 3519 m at Heishi near Dulan, Qinghai, China).