Bombus lapidarius ( Linnaeus, 1758 )

Williams, Paul H., Altanchimeg, Dorjsuren, Byvaltsev, Alexandr, Jonghe, Roland De, Jaffar, Saleem, Japoshvili, George, Kahono, Sih, Liang, Huan, Mei, Maurizio, Monfared, Alireza, Nidup, Tshering, Raina, Rifat, Ren, Zongxin, Thanoosing, Chawatat, Zhao, Yanhui & Orr, Michael C., 2020, Widespread polytypic species or complexes of local species? Revising bumblebees of the subgenus Melanobombus world-wide (Hymenoptera, Apidae, Bombus), European Journal of Taxonomy 719, pp. 1-120 : 71-74

Bombus lapidarius ( Linnaeus, 1758)

Figs 14 , 115–122 , 194

Apis Lapidaria Linnaeus, 1758: 579 .

Apis Audens Harris, 1776: 130 .

Apis Strenuus Harris, 1776: 131 .

Apis Opis Harris, 1776: 137 .

Apis Pertristis Harris, 1776: 137 .

Apis arbuʃtorum Fabricius, 1776: 246.

Apis coronata Geoffroy in Fourcroy, 1785: 449 .

Bremus truncorum Panzer, 1805: 85 .

Bremus regelationis Panzer, 1805: 56 .

Bombus albicans Schmiedeknecht, 1878: 405 .

Bombus lapidarius var. [subsp.] carpatiens Radoszkowski, 1884: 63.

Bombus lapidarius var. [subsp.] decipiens Pérez, 1890: 152.

Bombus luctuosus Ball, 1920: 32 (non Schmiedeknecht, 1878: 388 = B. pratorum (Linnaeus)) . Bombus lapidarius st. [subsp.] atlanticus Benoist, 1928: 212.

Bombus flavescens Knechtel, 1963: 712 , 714 (non Smith, 1852a: 45 = B. flavescens Smith ).

Bombus bisiculus Lecocq, Biella, Martinet & Rasmont, 2019: 7 . syn. nov.

Bombus lapidarius var. carpaticus – Friese 1905: 518, incorrect subsequent spelling.

Bombus lapidarium – Berezin, Beiko & Berezina 1996: 118, incorrect subsequent spelling.

Vogt (1909, 1911), Reinig (1935), and Lecocq et al. (2015, 2019) considered the taxon decipiens (thoracic dorsum with yellow bands) to be conspecific with the taxon lapidarius s. str. (thoracic dorsum black) as divergent regional colour patterns within a polytypic species.

Lecocq et al. (2015, 2019) considered B. caucasicus as likely to be a species separate from B. lapidarius from evidence of COI-coalescent analysis and from differences in the composition of male cephalic labial gland secretions (CLGS, believed to be sex pheromones).

Lecocq et al. (2013, 2015, 2019) also discovered divergence in CLGS between B. lapidarius from most of Europe and the yellow-banded bees in samples from southern Italy and they found this difference to coincide with a divergence in COI. They suggested that this (‘ decipiens -like’ taxon) might represent an ‘incipient’ species ( Lecocq et al. 2013) or a ‘recently diverged’ species ( Lecocq et al. 2019). Subsequently they published the name B. bisiculus for this taxon ( Lecocq et al. 2019).

Our PTP analysis ( Fig. 10 ) of coalescents in the COI gene supports three coalescents for candidate species within the lapidarius- group as identified in the four gene species tree ( Figs 21–22 ): a Caucasusregion candidate species, caucasicus , supported strongly, and two more widespread candidate species within the European taxon lapidarius s. lat. (a lapidarius- complex), supported relatively weakly. Our PTP results agree that the taxon decipiens and the taxon lapidarius s. str. are likely to be conspecific as parts of B. lapidarius s. lat. But our PTP results also show that there is a third candidate species ( Fig. 10 ) that is divergent in COI from B. lapidarius s. str. However, this candidate species does not correspond to (i.e., is not congruent or co-terminous with) Lecocq et al.’s (2015, 2019) south Italian taxon bisiculus (which is included in Figs 9–10). Our candidate species includes not only some of the yellow-banded samples from southern Italy described as the taxon bisiculus by Lecocq et al., but also (from the same data) some unbanded bees from Slovakia, the Czech Republic, Serbia, Bulgaria, and Hungary (Figs 9–10) that Lecocq et al. identify as the taxon lapidarius s. str. At present, our south-eastern candidate species is not supported as a separate species by integrative analysis because (1) not only is it much more broadly distributed than Lecocq et al.’s divergent south-Italian CGLS taxon bisiculus , but (2) so far we have been unable to find any diagnostic morphological characters, even in the colour pattern. Our south-eastern candidate species may represent the descendants of an isolated refugial population from the glacial period ( Reinig 1935; Lecocq et al. 2015), which appears now to be surrounded to the west and north by a second weakly divergent lineage, and to the east in Turkey by possibly a third weakly divergent lineage (Figs 9–10). So far this broader south-east European (but not Turkish) population can be identified only from COI sequences, so evidence would be needed from another character source to corroborate its current evolutionary independence before it could be accepted as a separate species. As well as showing only weak divergence among them in their COI barcodes, all of these lineages show very little variation within them, which corroborates them being relatively recent.

More work is needed to assess the variation within the lapidarius -complex in south-eastern Europe, but until further evidence is available from other character sources to corroborate consistent groups as separate species, we regard these bees tentatively as conspecific, as parts of a single widespread species, B. lapidarius s. lat.

Diagnosis

Females

Queens medium-sized body length 18–21 mm, workers 11–16 mm. Can be distinguished in Europe and West Asia by their combination of the hair on the face black with the hair on the thoracic dorsum either black or with some cream or yellow but not with pure white and not entirely yellow (cf. B. sichelii , B. eriophorus , B. incertus , B. alagesianus , B. semenovianus ). Queens can be distinguished (cf. B. simillimus ) by the combination of the hair of the thoracic dorsum black with the wings clear.

Males

Body length 11–16 mm. Can be distinguished in Europe and West Asia by their combination of the hair posteriorly on the thoracic dorsum and on T2 usually predominantly black and T4–7 bright red. Genitalia ( Fig. 194 ) with the gonostylus as long as broad, reduced as a rounded flat scale with the inner basal process reduced to a tooth (cf. rufipes- group, festivus- group, rufofasciatus -group); volsella with the inner distal corner broadly produced but without a narrow hook (cf. rufipes- group, festivus- group, rufofasciatus -group); penis valve head with the recurved inner hook just narrower than the narrowest part of the adjacent penis valve shaft (cf. B. eriophorus ); eye unenlarged relative to female eye.

Material examined

Holotype

SWEDEN • ♀ (queen), holotype of Apis lapidaria Linnaeus, 1758 ( Day 1979) ; Uppland; C. Linnaeus leg.; LSL (examined PW).

Material sequenced (29 specimens, includes some sequences from Lecocq et al. 2015)

FRANCE • 1 ♀ (worker); Aquitaine, Le Fontanaud ; 45.314° N, 0.346° E; 14 Aug. 2007; C. Ratti leg.; BOLD seq: 3771B12; PCYU: ML329 • 1 spec.; Eyne; 42.3024° N, 2.0106° E; M. Terzo leg.; GenBank seq: KC915850 ; UMONS: ML284 .

SWITZERLAND • 1 ♀ (worker); Valais, St Luc ; 46.2210° N, 7.6202° E; 22 Jul. 1999; P. Williams leg.; NHMUK seq: PW25 ; PW: ML186 .

RUSSIA • 1 ♀ (worker); Chuvashia, Cheboksari ; 56.1165° N, 47.244° E; 30 Jul. 2010, A. Lastukhin leg.; BOLD seq: SHMEL-E10; CSPU: ML330 .

MOROCCO • 1 spec.; Asni; 31.2499° N, 7.9833° W; K. Warncke leg.; GenBank seq: KJ572861 ; UMONS: ML193 .

SPAIN • 1 spec.; 39.4208° N, 0.8158° W; T. Lecocq leg.; GenBank seq: KC915889 ; UMONS: ML192 • 1 spec.; Camprodón ; 42.3136° N, 2.3719° E; D. Michez leg.; GenBank seq: KC915724 ; UMONS: ML274 • 1 spec.; Buñol ; 39.4208° N, 0.8158° W; T. Lecocq leg.; GenBank seq: KC915826 ; UMONS: ML275 • 1 spec.; Buñol ; 42.9511° N, 5.6578° W; T. Lecocq leg.; GenBank seq: KC915831 ; UMONS: ML276 .

IRELAND • 1 spec.; Dublin; 53.3414° N, 6.2769° W; R. Moermans leg.; GenBank seq: KC915738 ; UMONS: ML282 .

BELGIUM • 1 spec.; Nouvelles; 50.4144° N, 3.9794° E; T. Lecocq leg.; GenBank seq: KC915670 ; UMONS: ML278 .

FINLAND • 1 spec.; Nåt̂; 60.0464° N, 19.9731° E; B. Cederberg leg.; GenBank seq: KC915660 ; UMONS: ML277 .

AUSTRIA • 1 spec.; M̹hl; 47.5014° N, 10.7361° E; D. Michez leg.; GenBank seq: KC915689 ; UMONS: ML279 .

ITALY • 1 spec.; S. Margherita; 44.7158° N, 9.2087° E; M. Cornalba leg.; GenBank seq: KC915719 ; UMONS: ML281 • 1 spec.; Salcito ; 41.7447° N, 14.5147° E; T. Lecocq leg.; GenBank seq: KC915714 ; UMONS: ML194 • 1 spec.; Cellara ; 39.215° N, 16.3825° E; T. Lecocq leg.; GenBank seq: KC915871 ; UMONS: ML271 • 1 spec.; Villadoro ; 37.6814° N, 14.3047° E; T. Lecocq leg.; GenBank seq: KC915876 ; UMONS: ML272 • 1 spec.; Piano Provenzana ; 37.7994° N, 15.0647° E; T. Lecocq leg.; GenBank seq: KC915881 ; UMONS: ML273 .

SLOVENIA • 1 spec.; Studenčice; 46.3722° N, 14.1575° E; T. Lecocq leg.; GenBank seq: KC915710 ; UMONS: ML386 .

UKRAINE • 1 spec.; Lastiosti; 48.7172° N, 24.525° E; D. Michez leg.; GenBank seq: KC915844 ; UMONS: ML283 .

TURKEY • 1 ♀ (worker); Erzingan, Yeniyol-Ahmitli ; 39.8926° N, 39.3676° E; 5 Aug. 2002; H. Hines leg.; BOLD seq: 6877H02; SC: ML418 • 1 ♀ (worker); Erzingan, Yeniyol-Ahmitli ; 39.8926° N, 39.3676° E; 5 Aug. 2002; H. Hines leg.; BOLD seq: 6877H03; SC: ML419 .

SERBIA • 1 spec.; Belgrade; 44.7872° N, 20.4517° E; A. Cetkovic leg.; GenBank seq: KC915752 ; UMONS: ML387 .

CZECH REPUBLIC • 1 spec.; Praha; 50.105° N, 14.4167° E; T. Lecocq leg.; GenBank seq: KC915695 ; UMONS: ML408 .

SLOVAKIA • 1 spec.; Nitra; 48.3036° N, 18.1539° E; T. Lecocq leg.; GenBank seq: KC915797 ; UMONS: ML410 .

HUNGARY • 1 spec.; Szentendre; 47.6633° N, 19.0719° E; T. Lecocq leg.; GenBank seq: KC915700 ; UMONS: ML409 • 1 spec.; Gárdony; 47.2011° N, 18.6442° E; T. Lecocq leg.; GenBank seq: KC915800 ; UMONS: ML411 .

BULGARIA • 1 spec.; Beklemeto; 42.7789° N, 24.6142° E; T. Lecocq leg.; GenBank seq: KC915704 ; UMONS: ML280 • 1 spec.; same collection data as for preceding; GenBank seq: KC915802 ; UMONS: ML407 .

Global distribution

(European widespread grassland, often lowland, species extending into the margins of North Africa and West Asia) North Africa: MOROCCO. – Europe: SPAIN, UK, IRELAND, FRANCE, BELGIUM, NETHERLANDS, DENMARK, GERMANY, POLAND, SWEDEN, FINLAND, SWITZERLAND, AUSTRIA, CZECH REPUBLIC, SLOVAKIA, ITALY, HUNGARY, ROMANIA, BULGARIA, SLOVENIA, SERBIA, ALBANIA, MONTENEGRO, MACEDONIA, GREECE, UKRAINE, RUSSIA: European Russia, Crimea, Ural. – West Asia: TURKEY. (NHMUK, PW, ZMHB.) The species is widespread and often abundant.

The distribution of this species is known to extend eastwards into Russia as far as Arkaim Nature Reserve, Chelyabinsk Oblast (AB: 52.65° N, 59.60° E).

Behaviour

Colonies of this species have been described ( Alford 1975; Benton 2006; Goulson 2010). Food-plant generalists ( Alford 1975; Rasmont 1988; Benton 2006; Goulson 2010). Male mate-searching behaviour is patrolling ( Alford 1975; Benton 2006; Goulson 2010).

Figures

Figs 14‒16. Maps of sequenced samples as in Figs 12–13. 14. The tanguticus-group and the lapidarius- group. 15. The sichelii-group. 16. The keriensis-group.

Figs 103–138. Simplified diagrams for the colour patterns of the hair on the dorsum for the species from the integrative analysis. The dorsum is divided into regions, each of which shows only the predominant or most apparent colour for that region using a simplified colour palette, with olive indicating a mixture of black and yellow hair, and grey indicating a mixture of black and white hair. The tanguticus-group. 103. Worker, China-Qinghai. 104. Worker, China-Qinghai. 105. Queen, China-Qinghai. 106. Queen, China-Xizang. 107. Queen, India-Kashmir. The lapidarius-group. 108. Queen, Russia-North Ossetia. 109. Worker, Azerbaijan. 110. Queen, Georgia. 111. Male, Russia-North Ossetia. 112. Male, Russia-North Ossetia. 113. Male, Russia-North Ossetia. 114. Male, Turkey. 115. Queen, Morocco. 116. Queen, Spain. 117. Queen, Spain. 118. Queen, UK. 119. Male, Spain. 120. Male, Spain. 121. Male, UK. 122. Male, UK. The sichelii-group. 123. Queen, Iran. 124. Male, Iran. 125. Queen, India-Kashmir. 126. Queen, India- Kashmir. 127. Male, India-Kashmir. 128. Male, India-Kashmir. 129. Queen, Iran. 130. Queen, Russia- Sakha. 131. Queen, China-Sichuan. 132. Worker, China-Sichuan. 133. Queen, Mongolia. 134. Worker, Mongolia. 135. Queen, Spain. 136. Worker, Austria. 137. Male, Turkey. 138. Male, Mongolia.

Figs 190‒198. Morphology of the male genitalia for species of the subgenus Melanobombus von Dalla Torre, 1880 from the dorsal aspect, anterior at the bottom of the image, posterior at the top. 190. Bombus friseanus Skorikov, 1933, China-Yunnan. 191. B pyrosoma Morawitz, 1890, China- Beijing. 192. B. formosellus (Frison, 1934), China-Taiwan. 193. B. eriophorus Klug, 1807, Russia- North Ossetia. 194. B. lapidarius (Linnaeus, 1758), UK. 195. B. incertus Morawitz, 1881, Turkey. 196. B. semenoviaus (Skorikov, 1914), India-Kashmir. 197. B. sichelii Radoszkowski, 1859, Austria. 198. B. ladakhensis Richards, 1928, China-Sichuan. Scale bars = 1 mm.

Fig. 10. October 2019 (Fig. 8) Bayesian PTP analysis of MrBayes tree of unique COI barcodes (UHF- PTP). Symbols as in Fig. 9.

Fig. 21. A sample of 10 000 species trees from among 100 million trees for species of the subgenus Melanobombus von Dalla Torre, 1880 reconstructed with *BEAST from gene trees for the COI, 16S, opsin and PEPCK genes, displayed in green using Densitree, with the summary ‘root canal’ superimposed as a thick blue line. The outgroup B. nobilis Friese, 1905 is shown.

Fig. 22. Most likely dated phylogenetic (ultrametric) tree for the species of the subgenus Melanobombus reconstructed von Dalla Torre, 1880 with *BEAST from trees for four genes (COI, 16S, PEPCK, opsin) with B. nobilis Friese, 1905 as the outgroup (not shown), estimated as the maximum-clade-credibility tree among a sample of 10 000 species trees with a 1% burn-in out of 100 million MCMC trees. Values above the nodes are Bayesian posterior probabilities showing support for groups. Values below the nodes are estimated dates of divergence in Ma (millions of years before the present) calibrated from a molecular estimate for the date of crown divergence within the subgenus Melanobombus. Grey bars show the 95% confidence limits on the estimated dates of divergence. Species groups discussed in the text are labelled in circles: rp = rufipes-group; fs = festivus-group; rf = rufofasciatus-group; tg = tanguticus-group; la = lapidarius-group; si = sichelii-group; and ke = keriensis-group.