Bombus avinoviellus (Skorikov)

Williams, Paul H., Huang, Jiaxing, Rasmont, Pierre & An, Jiandong, 2016, Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species’ gene coalescents and morphology (Hymenoptera, Apidae), Zootaxa 4204 (1), pp. 1-72 : 41-43

6. Bombus avinoviellus (Skorikov)

( Figs 3 , 16 , 29 , 46 , 61 )

Mendacibombus avinoviellus Skorikov 1914:126 , type-locality citation (Cyrillic) ‘[along the river Sind above Sonamarg, … Baltal … pass Zodji-La]’. Lectotype queen by present designation ZISP examined, ( Cyrillic ) ‘[along the river Sind upstream of Sonamarg ]’ ( Great Himalaya , Kashmir, India). Note 1.

[ Mendacibombus avinoviellus var. eriophoroides , var. cremeus Skorikov 1914:126 , infrasubspecific.] Bombus niveatus <subsp.> callophenax Cockerell 1917:122, type-locality citation ‘Kashmir’. Holotype queen by monotypy USNM examined ( Williams , 1991), ‘ Kashmir’ ( Kashmir , India). Synonymised with Bombus avinoviellus (Skorikov) by Williams (1991).

Mendacibombus avinoviellus Skorikov; Skorikov 1923 :149; Skorikov 1933:2.

Bombus (Mendacibombus) avinoviellus (Skorikov) ; Richards 1930:635; P.H. Williams 1991:39; P.H. Williams & Cameron 1993:126; P.H. Williams 1998:99; P.H. Williams 2004:no. 25; Cameron et al. 2007:165; Suhail et al. 2009:3 [not seen]; P.H. Williams et al. 2010:124.

[ Bombus (Mendacibombus) avinoviellus Var. nov. subtunicatus Richards, 1930:635, infrasubspecific.]

[ Mendacibombus afghanus (Reinig) ; Tkalců 1969:193, misidentification: see below.]

Bombus (Sibiricobombus) avinoviellus (Skorikov [cited as Cockerell]); Burger et al. 2009:457.

Bombus avinoviellus (Skorikov) ; Sabir et al. 2011:160 [not seen].

Note 1 ( avinoviellus ). Skorikov’s original description of several females of the taxon avinoviellus cites the type locality as the Sind valley above Sonamarg up to the Zoji-La pass in the Great Himalaya. The ZISP collection studied by Skorikov contains a queen that agrees with the original description and carries the labels: (1) white, handwritten ( Cryrillic ) ‘[[ Along the river Sindu, upstream of] / Sonomarga, 2400‒3000 mt / G. Jakobson] 9‒10.VI.12 ’; (2) white, printed (Cyrillic) ‘[k. Skorikova]’; (3) red, printed ‘ Holotypus ’; (4) white, handwritten ‘avinoviellus’; (5) red, handwritten ‘ Lectotypus Mendaci- / Bombus avinoviel- / lus Skorikov / design. Podbolotsk. ’ (M. Podbolotskaya, unpublished); (6) green, printed ‘ Mendacibombus / MD# 3528 det. PHW’; (7) red, printed ‘ LECTOTYPE [female] / Mendacibombus / avinoviellus / Skorikov, 1914 / det. PH Williams 2012’; (6) white, printed ‘[female] Bombus / ( Mendacibombus ) / avinoviellus / 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.

A second queen collected at Baltal on the upper Sind river by Jakobson in 1912 (MD#598, NHM, sent by Skorikov as part of an exchange with the NHM in 1934), which is closely similar in morphology, is designated here as a paralectotype and is interpreted as conspecific.

Etymology. The species is named after A. Avinoff, a Russian entomologist who prior to 1914 had been collecting in Central Asia. After the Russian revolution he emigrated to the USA and later became Director of The Carnegie Museum.

Taxonomy and variation. The interpretation of this species is based here on the form of the female clypeus and labrum and of the male genitalia (and between species on DNA). This disagrees with earlier concepts ( Tkalců, 1969), diagnosed originally in terms of the hair colour pattern ( Skorikov, 1910b), because the species appears to be much more variable in colour pattern than was previously understood.

Skorikov (1914) described females of the taxon avinoviellus s. str. from the Kashmir Great Himalaya as having all of the pale bands grey-white, with an indistinctly-delimited black band between the wing bases (MD#3528). The taxon callophenax has a similar colour pattern with only a slightly more distinct black band between the wing bases. In the mountains around the Vale of Kashmir, the black band between the wings varies from broad and distinct (MD#405) to almost absent, as a small black spot (MD#397).

Our COI tree shows that specimens from further east in the Himalaya (Uttarakhand MD#286 and Nepal MD#265, 266) have a similar but undescribed colour pattern in which the pale bands are brownish yellow. These have very short branch lengths between them and specimens of the taxon avinoviellus s. str. ( Fig. 13 : the yellowbanded taxon ‘yellowbanded’ MD#265, 266, 286 and the white-banded taxon avinoviellus s. str. MD#3863). The yellow-banded individuals are interpreted here as conspecific, as parts of B. avinoviellus s. l.. Individuals from north-western Kashmir, in Pakistan, are also yellow-banded. Some individuals from Gulmarg and similar sites in the outer Pir Panjal range appear to be intermediate, with white hair on the thorax but yellow hair on T1‒2. Grouping of specimens with these three colour patterns is supported by the associated males, which match in being yellow- or white-banded and in sharing the same diagnostic form of the male genitalia. For this COI group B. avinoviellus s. l., the form of the female labrum and clypeus is also diagnostic.

Williams (1991) reports a specimen (MD#732) from Banidas, Pakistan (in the Karakorum mountains at the north-western end of the range), that is morphologically closely similar to B. avinoviellus , but which has a colour pattern of the hair similar to B. marussinus . This, and two further specimens from the same site with a similar colour pattern (MD#4058, 4059), were in Tkalců’s collection (recently transferred to OLL) have now been examined. The darker wings, predominantly black hair of T6, and colour pattern of these specimens match the description of a series of specimens from the Karakorum by Tkalců (1969), misidentified (we believe) under the name Mendacibombus afghanus (see the comments on B. marussinus ). No male specimens with this unbanded yellow colour pattern are known from this region from which to check their distinctive genital morphology. The samples MD#4058, 4059 were sequenced, but yielded fragments with only the first 96 bp. Of the six uniquely diagnostic nucleotides for B. avinoviellus ( Table 5), only those at positions 34(A) and 79(A) are within this fragment, but both of these samples match B. avinoviellus at both positions. In contrast, diagnostic nucleotides within this range for the other nine species of Mendacibombus show no other complete matches, with only partial matches (1/2 diagnostic nucleotides) for two species: B. waltoni (position 22A) and B. margreiteri (position 59C). Both species are morphologically distinctly different from B. avinoviellus . Consequently, these results are consistent with the yellow unbanded bees being parts of B. avinoviellus , possibly as an ancestral colour pattern shared with B. marussinus .

Diagnostic description. Wings lightly clouded with brown (cf. B. himalayanus , B. marussinus ). Hair short, even and dense. Female hair colour pattern: generally black, but with pale hair (yellow and/or grey-white) intermixed especially as short hairs on the face, in a transverse band anteriorly on the thoracic dorsum and extending laterally and ventrally as white hair to the midleg base, in a transverse band posteriorly on the thoracic dorsum (scutellum; so the thoracic dorsum between the wing bases may have the hair entirely black, but usually has black and many pale hairs strongly intermixed, cf. B. himalayanus and B. marussinus , or sometimes with the pale hairs predominant), on T1, on T2 anteriorly and medially (T1 is more often yellow than T2 and the thoracic bands, so that individuals often have both yellow and white) or more rarely all of T2 pale except for a few black hairs intermixed medially along the posterior margin, T3 varying from orange only as a narrow posterior fringe to orange except for some black hairs anteriorly, and T4‒6 orange, T6 medially with black hair and often entirely black. Hindleg tibia with the corbicular fringes black, often a few hairs with orange tips. Female morphology: labrum with the basal depression very broad, the transverse ridge narrower medially than the basal depression, in the median third consistently convex throughout, not subsiding or interrupted and with few scattered punctures, slightly angled between the lateral ends, the lateral tubercles with few punctures ( Fig. 16 ) (cf. B. himalayanus , B. marussinus ). Clypeus in its central half with few scattered punctures, many more small than large punctures (cf. B. marussinus ), the small punctures spaced by about their own widths (cf. B. himalayanus ), the anterior depressions with a broad band of dense punctures that are many punctures in breadth (cf. B. himalayanus ). Male morphology: genitalia ( Fig. 29 ) 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 strongly dorso-ventrally flattened and plate-like. 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 strongly laterally compressed.

Material examined. 31 queens 74 workers 70 males, from India, Nepal, and Pakistan ( Fig. 61 : NHM, NME, OLL, PW, RR, ZISP), with 8 specimens sequenced (interpretable sequences listed in Figs. 11–13 ).

Habitat and distribution. Flower-rich alpine and subalpine grassland, at elevations 1881‒(2796)‒ 4080 m a.s.l.. A species of the Karakorum and west Himalayan mountains. Compared to B. himalayanus , the distribution of B. avinoviellus extends slightly less far to the north but further to the east and it tends to occur at lower elevation (the two species rarely occur together). Bombus avinoviellus replaces the eastern B. convexus in the lower alpine zone and wetter upper forest meadows of the western Himalaya. Regional distribution maps are available for Kashmir ( P.H. Williams 1991) and Nepal (P.H. Williams et al. 2010). The unbanded yellow taxon from the Karakorum appears to be very rare.

Food plants. Williams (1991).

Behaviour. Williams (1991), mate-searching male shown in Fig. 3.

Figures

FIGURE 13. Assigning names to species from an estimate of phylogeny for 130 COI sequences of the subgenus Mendacibombus. Based on a BEAST analysis of the 30 unique haplotypes (Fig. 11), with the remaining sequences interpolated back into the tree with 0 branch lengths from their matching samples (where a sequence matches more than one longer sequence within a species in the Collapse results, it is added after the first matching sequence, with the addition of the two short-sequence yellow unbanded specimens from Pakistan, MD # 4058, 4059). The sequence labels follow the format used in Figs 11, 12. Lineages accepted as species from the GMYC models (Fig. 11) are shown as thick branches, the most recent common ancestors of each species are shown with a black spot, and branches within species are shown as thin branches. Asterisks mark samples used as informal proxies for the type specimens of each of the taxon names (Table 1). The proxy sample for the type specimen for the oldest available name (the valid name) for each species (from Fig. 11) is marked in bold. The interpretations of the species with their valid names are shown in grey to the right.

FIGURES 1 ‒ 6. Views of perching males of species of the subgenus Mendacibombus, showing the anteriorly extended antennae and laterally extended wings that are characteristic of their form of male mate-searching behaviour: 1, B. waltoni at Diebu ca 3910 m, Minshan mountains, Gansu, China, 29. viii. 2009; 2, B. convexus at Diebu ca 3340 m, Minshan mountains, Gansu, China, 29. viii. 2009; 3, B. avinoviellus at Gulmarg ca 2700 m, Pir Panjal mountains, Kashmir, India, 16. viii. 1985; 4, B. himalayanus at Apharwat ca 4100 m, Pir Panjal mountains, Kashmir, India, 30. viii. 1986; 5 ‒ 6, B. margreiteri near Dulan ca 3520 m, Burhan Budai mountains, Qinghai, China, 31. viii. 2010. Photos by PW (Figs 3 – 4 are the best available for these species).

FIGURES 15 ‒ 23. Morphology of the female (queen) head from the ventral aspect (labrum and mandibles): 15, B. marussinus queen, Pakistan MD # 482; 16, B. avinoviellus queen, India MD # 598; 17, B. turkestanicus queen, Tajikistan MD # 320; 18, B. defector queen, Kyrgyzstan MD # 1080; 19, B. margreiteri queen, Mongolia MD # 319; 20, B. himalayanus queen, India MD # 453. Morphology of the female (queen) left hindleg tibia from the left lateral aspect, dorsal at the top of the image, anterior to the left: 21, B. defector, China MD # 1251; 22, B. margreiteri, Mongolia MD # 319; 23, B. turkestanicus, Kyrgyzstan MD # 324.

FIGURES 24 ‒ 35. Morphology of the male genitalia for species of the subgenus Mendacibombus from the dorsal aspect, anterior to the left of the image, posterior to the right: 24, B. superbus, China MD # 339; 25, B. waltoni, China MD # 216; 26, B. convexus, China MD # 215; 27, B. makarjini, Kazakhstan MD # 1240; 28, B. marussinus, Pakistan MD # 408; 29, B. avinoviellus, India MD # 404; 30, B. himalayanus, India MD # 426; 31, B. turkestanicus, China MD # 351; 32, B. defector, Kyrgyzstan MD # 367; 33, B. margreiteri, China MD # 294; 34, B. handlirschianus, Russia MD # 835; 35, B. mendax, Spain MD # 689.

FIGURES 36 ‒ 55. Morphology of parts of the male genitalia from the dorsal aspect of the left side, anterior to the left of the image, posterior to the right, white bars indicating morphological characters referred to in the key to males: 36, B. waltoni; 37, B. mendax; 38, B. superbus; 39, B. convexus; 40, B. waltoni; 41, B. convexus; 42, B. defector; 43, B. mendax; 44, B. mendax; 45, B. turkestanicus; 46, B. avinoviellus; 47, B. mendax; 48, B. mendax; 49, B. makarjini; 50, B. handlirschianus; 51, B. himalayanus; 52, B. turkestanicus; 53, B. himalayanus; 54, B. himalayanus; 55, B. marussinus.

FIGURES 56 ‒ 67. Maps of the global distributions of species of the subgenus Mendacibombus from the material examined, with grey spots for specimen records and black spots for the samples with COI sequences (each species is unknown from regions outside the map boundaries shown); grey crosses for records of all species of Mendacibombus combined. Relief map with hill shading, Cartesian orthonormal projection, grey lines show borders to national administration according to UN maps, north at the top of the map. Image created in ArcGIS using World _ Shaded _ Relief basemap © 2014 Esri.

FIGURES 11 ‒ 12. Recognising species from an estimate of phylogeny for 30 unique COI haplotypes of the subgenus Mendacibombus by BEAST, using GMYC models and the PTP procedure. From the GMYC models (11), the single threshold T is shown by the vertical grey bar so that the intersecting lineages are interpreted as indicating 12 separate species (black spots at coalescent nodes; outgroups not shown). Values below the nodes of the maximum clade-credibility tree are Bayesian posterior probabilities showing branch support (groups with values <0.8 are considered unreliable) from the BEAST analysis with two billion MCMC generations and a 1 % burn-in. The x - scale axis is calibrated in substitutions per nucleotide site. From the PTP procedure (12), the Bayesian PTP solution with highest support also indicates 12 species. Values above the nodes are PTP Bayesian support values that all daughter haplotypes are parts of a single species; values below the nodes are Bayesian posterior probabilities showing branch support. The scale bar is calibrated in substitutions per nucleotide site. Each unique haplotype is represented by one of the longest available sample sequences, labelled with: the sequence length in number of base pairs, a taxon name or name for an unpublished colour pattern (light / dark / yellow / white / pale), and then a code that consists of a specimen identifier (MD #) from the project database and (after the hyphen) a sample identifier from BOLD or from GenBank, followed with its geographic origin.

FIGURE 7. Frequency of specimen collection by decade among specimens examined for species of the subgenus Mendacibombus excluding B. mendax and B. handlirschianus.