A simplified subgeneric classification of the bumblebees

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A simplified subgeneric classification of the bumblebees(genus Bombus)

Paul H. Williams, Sydney A. Cameron, Heather M. Hines, Bjorn Cederberg,Pierre Rasmont

To cite this version:Paul H. Williams, Sydney A. Cameron, Heather M. Hines, Bjorn Cederberg, Pierre Rasmont. Asimplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, Springer Verlag,2008, 39 (1), pp.46-74. �hal-00891940�

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Apidologie 39 (2008) 46–74 Available online at:© INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.orgDOI: 10.1051/apido:2007052

Original article

A simplified subgeneric classification of the bumblebees(genus Bombus)*

Paul H. Williams1, Sydney A. Cameron2, Heather M. Hines2, Bjorn Cederberg3,Pierre Rasmont4

1 Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK2 Department of Entomology, University of Illinois, Urbana, IL 61801, USA

3 Swedish Species Information Centre, University of Agricultural Sciences, PO Box 7007, 750 07 Uppsala,Sweden

4 Laboratory of Zoology, University of Mons-Hainaut, Avenue Maistriau 19, 7000 Mons, Belgium

Received 26 June 2007 – Revised 14 October 2007 – Accepted 15 October 2007

Abstract – A system of subgenera has been widely used for nearly a century to communicate ideas ofrelationships among bumblebee species. However, with 38 subgenera in recent lists for about 250 species,the system has come to be seen as too complicated. In this paper we suggest four criteria to guide the processof simplifying the subgeneric system, so that ideally subgenera should become: (1) monophyletic; (2) fewer;(3) diagnosable from morphology; and (4) names for important behavioural and ecological groups. Usinga new strongly-supported estimate of phylogeny for almost all bumblebee species, we apply these criteriato reduce the system to 15 subgenera, and we assess the consequences. Ten new subgeneric synonyms arerecognised. Keys to identify adult bumblebees to the simplified subgenera are provided for both sexes.

bumblebee / Bombus / subgenera / phylogeny / classification

1. INTRODUCTION

Bumblebees are a group of about 250species, now placed in a single genus, Bom-bus (Latreille, 1802). To summarise variouskinds of relationships among these species,a system of subgenera has been developedover the last century (e.g. Dalla Torre, 1880;Radoszkowski, 1884; Robertson, 1903; Vogt,1911; Skorikov, 1914, 1923; Krüger, 1920;Richards, 1929) and is now in common use.A review of the history of the developmentof bumblebee subgeneric systems is given byIto (1985), while a unified world list of sub-generic names with their included species issummarised by Williams (1998), and keys torecently accepted subgenera are provided by

Corresponding author: P.H. Williams,[email protected]* Manuscript editor: E.A.B. Almeida

Richards (1968) and Michener (2000, 2007).Now that we have a strongly supported esti-mate of relationships among almost all bum-blebee species world-wide (Cameron et al.,2007), some minor revision will be unavoid-able to ensure that the subgeneric nomencla-ture recognises only monophyletic groups.

However, the recent form of the bumble-bee subgeneric system (e.g. as summarisedby Michener, 2000, 2007) is widely regardedas unnecessarily complicated. This is exac-erbated because the keys to subgenera aredifficult to use and do not work well formany species. Consequently, a simplifica-tion of the subgeneric system is desirable(Kruseman, 1952; Milliron, 1961; Menke andCarpenter, 1984; Williams, 1998; Michener,2000; Cameron et al., 2007). When using thenew estimate of phylogeny to ensure mono-phyletic subgenera, we have an opportunity

Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2007052

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Bumblebee subgenera 47

to make a more extensive rationalisation ofthe system. Previous attempts to make radicalchanges (Milliron, 1961; Tkalcu, 1972) havebeen largely ignored because their advantageswere not widely appreciated (e.g. Richards,1968; Michener, 2000), and because the sub-generic keys (Milliron, 1971, 1973a, b) wereeven more difficult to use.

In this paper, we identify the principal pur-poses for which bumblebee subgenera are use-ful and then examine how we might modifythe subgeneric system to make it better suitedto meeting explicit and widely held aims.

2. AIMS

Bumblebee subgenera could be useful inmeeting three main aims:

1. to reflect and be consistent with phyloge-netic relationships;

2. to aid identification, as a stepping stone toidentifying species (especially importantwhen dealing with unfamiliar or poorlyknown faunas); and

3. to predict (interpolate) poorly sampled be-havioural and ecological characteristics.

The primary aim in using bumblebee sub-genera has changed through time. Formalsubgeneric names were first introduced forbumblebees by Dalla Torre (1880, 1882), orig-inally to group bees with similar colour pat-terns. Radoszkowski (1884) used informalspecies-group names, but applied them in-stead to groups of species recognised formorphological similarities in their male gen-italia. This morphological system was thenlargely re-invented by Vogt (1911), who in-troduced his own set of formal subgenericnames. Skorikov (e.g. 1914, 1922, 1923, 1931)adopted Vogt’s system and names and thengreatly elaborated it, establishing most of thecurrent subgeneric system (although as a mixof subgeneric and generic names, in manycases published without descriptions or di-agnoses). Skorikov also extended the role ofbumblebee subgenera to discussing phylogenyand the evolution of behaviour, ecology, anddistribution patterns, a subject of interest tomany recent researchers (e.g. Hobbs, 1964;

Williams, 1985; Cameron and Williams, 2003;Kawakita et al., 2004; Hines, in press). Someauthors, while recognising subgenera, have fo-cussed instead on a few much larger groups or‘sections’, either when considering morphol-ogy (Robertson, 1903; Krüger, 1917; Frison,1927), or when considering behaviour andecology (Sladen, 1912; Plath, 1927, 1934).According to the International Code of Zo-ological Nomenclature (ICZN, 1999: Article10.4), if only a single genus of bumblebees isto be recognised and if these section names arerequired for use as formal names below therank of genera, then they have to be treatedas names for taxa at the rank of subgenera(Williams, 1998).

However, subgenera are no longer neededfor communicating ideas of phylogenetic rela-tionship among bumblebees. The use of treediagrams for summarising relationships hasthe advantage over subgenera that trees canshow many more levels of grouping or phylo-genetic clades. Authors of subgenera had triedto keep track of the improving knowledge ofmorphology and concepts of relationship asbumblebees became better known world-wideby splitting subgenera to recognise progres-sively finer divisions. This has caused prob-lems because the pattern of splitting subgen-era has become highly asymmetric and manysubgenera (11 of 38) are monotypic. Theseconvey little information on relationships. Tosome extent this asymmetry is inevitable be-cause phylogenetic trees are rarely symmet-ric. But in some cases the problem goes be-yond this. In one example (Williams, 1998),there are two large clades that occur in bothNorth and South America: a broad fervidus-group and a broad robustus-group, each with20 species. But whereas the former clade hasbeen treated recently as a single subgenus, thelatter clade has been split into 10 subgenera.

Similarly, subgenera might appear to havebeen superseded by phylogenetic trees whenseeking to communicate the distribution ofcharacter states among species. Trees have of-ten been used to map the evolution of charac-ters (e.g. Krüger, 1920; Kawakita et al., 2004;Cameron et al., 2007; Hines, in press). In ad-dition, trees mapped with illustrations of mor-phological characters (e.g. Williams, 1985: his

48 P.H. Williams et al.

Fig. 6) could, at least in principle, be used asan aid (or key) for species identification, al-though this has not been used in practice forbumblebees.

Nonetheless, subgenera have real advan-tages. Some discussions of bumblebee ecol-ogy continue to find subgeneric names usefulas short-hand pointers to groups with particu-lar behavioural and ecological characters (e.g.Hobbs, 1964; Sakagami, 1976; Plowright,1977). It is more convenient for field biologiststo remember names for a few large clades ofspecies with characteristic behaviour and ecol-ogy, rather than having to remember an en-tire phylogenetic tree with all of the charactersmapped upon it. Second, phylogenetic treesare often unsuited for use to structure routineidentification aids, because not all clades con-veniently share easily observed and unambigu-ous morphological characters (see below). De-cisions in traditional identification keys havetheir pathways set by the authors (Walter andWinterton, 2007). They can be ordered prag-matically to minimise the risk of misidentifi-cation, with the least ambiguous characters intheir earlier couplets. These keys frequentlyuse subgenera as a convenient intermediatestage or stepping stone to species identifica-tion (e.g. Pittioni, 1939; Løken, 1973; Thorpet al., 1983). But above all, subgeneric nameshave the advantage over generic names thatthey can be ignored by non-specialists who donot need to use them. Subgeneric names canstill be used by specialists when they find themhelpful.

3. CRITERIA

From the aims listed above, we can iden-tify four criteria that should be useful to guidechanges to the bumblebee subgeneric system.Subgenera should become:

1. monophyletic;2. fewer;3. diagnosable from morphology;4. names for principal behavioural and eco-

logical groups.

Not all of these criteria are easy to satisfy,and the advantages of any changes must be

balanced against the cost of instability fromfrequent changes. When moving from generalaims to specific operational criteria, there arealso potential conflicts among the criteria, asdiscussed below.

Monophyly. This is widely accepted as aminimum requirement of higher taxa such assubgenera and is more important than stabil-ity. Recent estimates of bumblebee phylogeny(Cameron et al., 2007) show that not all cur-rent subgenera are monophyletic, and indeedsome are polyphyletic. Because the supportingevidence is strong, we feel obliged to modifythe subgeneric system to avoid polyphyly. Fur-thermore, we prefer strict monophyly over pa-raphyly because it ensures that classificationsare most likely to be predictive for those char-acters not used in their construction (whetherof morphology, behaviour, or ecology), be-cause of the underlying evolutionary model ofdescent with modification (e.g. Kitching et al.,1998). Because there are many possible waysof modifying the system while ensuring mono-phyly, it is useful to identify subsidiary criteriathat help to achieve the greatest overall benefit.

Fewer. The precise choice of level withina phylogenetic tree for labelling a supraspe-cific taxon with a particular nomenclaturalrank is essentially arbitrary, and there is alarge literature discussing this problem (e.g.Stevens, 2006). For bumblebees, there is abroad perception that there are too many sub-genera and that a substantial reduction in theirnumber would be desirable (Kruseman, 1952;Milliron, 1961; Menke and Carpenter, 1984;Williams, 1998; Michener, 2000; Cameron etal., 2007). Given a well-resolved and stronglysupported estimate of bumblebee phylogeny,then the number of subgenera can be re-duced while remaining consistent with mono-phyly. Among a small e-mail poll of bum-blebee ecologists in Europe and North Amer-ica (12 respondents), the idea of a reducednumber of larger subgenera was supported en-thusiastically. The primary criterion of mono-phyly requires that some monotypic subgenera(Kallobombus) or small subgenera (Bombias)continue to be recognised (Cameron et al.,2007). Reducing the number of subgenerawould not prevent authors from recognising


informal species groups in an ad-hoc mannerwhen necessary.

Morphological diagnosability and be-havioural/ecological groups. Conflicts amongcriteria might arise particularly if behaviouraland ecological characteristics were associatedwith clades that were established from DNAevidence but which have no known diagnosticmorphological characters (a phenomenonfamiliar from work on the higher classifica-tion of plants, e.g. Stevens, 2006). This isthe most serious challenge to our efforts torecognise useful subgenera for bumblebees.It can be studied by plotting the distributionof morphological/behavioural/ecological cha-racters on phylogenetic trees and looking forconcentrations of character-state changes atparticular nodes (which is not necessarilythe same as long branch lengths based onDNA divergences). We find that many smallterminal groups of bumblebee species areeasily diagnosed by morphological characters,but in some parts of the tree there remainsa morass of relatively undifferentiated more‘basal’ species (this is particularly a prob-lem with early-diverging species within theproposed broader concepts of the subgen-era Thoracobombus, Melanobombus, andCullumanobombus, see below). One solutionis to recognise paraphyletic ‘stem’ groups,although this has been avoided here. An-other possible solution would be to ignorebehaviour and ecology and maintain thetraditional precedence of morphologicaldiagnosability as the criterion for recognisingsubgenera. We choose to exclude geograph-ical distribution from use as a character,because biogeography cannot be analysed forsubgenera if distribution is used in their diag-nosis without the logic of the biogeographicanalysis becoming circular. Concentratingon morphological diagnosability allows sub-genera to be more useful in an intermediatestage in the identification process. Precedenceof morphological diagnosability should alsopromote nomenclatural stability, because mor-phology can largely be known now, whereaswe can only hope that our patchy currentknowledge of behaviour and ecology world-wide (e.g. Sakagami, 1976) will improvein the future. Fortunately, at least in some

cases, behavioural and ecological groups docorrespond conveniently to morphologicallydiagnosable subgenera (see the Assessmentsection).

4. APPLICATION

Monophyly of subgenera should now beachievable because we have a highly resolvedestimate of phylogeny for almost all bumble-bee species that is strongly supported by evi-dence from the DNA sequences of five genes(Cameron et al., 2007; largely compatible withmore restricted DNA analyses by Pedersen,2002; Cameron and Williams, 2003; Kawakitaet al., 2003; Hines et al., 2006). Here we usea tree redrawn from Cameron et al. (2007:their Fig. 2), which recognises only the cladeswith the strongest support (Bayesian posteriorprobabilities � 0.95, Fig. 1) at or above therank of the existing subgenera.

For most of the last two centuries, mostauthors have placed bumblebees in two gen-era: Bombus (for the truly social species)and Psithyrus (for the cuckoo bumblebees,all obligate social parasites of other bumble-bees). Both morphological and molecular ev-idence shows that a genus Bombus exclud-ing Psithyrus is paraphyletic (Williams, 1995;Cameron et al., 2007), a situation that shouldbe avoided (see above). If all bumblebees, in-cluding the parasitic species, were to be in-cluded in a single genus Bombus, this wouldhave the advantage that it emphasises boththe many shared homologies of the group, onthe one hand, and the shared differences fromother groups of corbiculate bees, on the other.This proposal (Williams, 1991) has gainedwidespread acceptance and stability.

Psithyrus has been split previously byFrison (1927), Popov (1931) and Pittioni(1949) into eight smaller subgenera (Psithyrusin the narrow sense, plus Allopsithyrus, Ash-tonipsithyrus, Ceratopsithyrus, Eopsithyrus,Fernaldaepsithyrus, Laboriopsithyrus, Metap-sithyrus, see Williams, 1998). These smallersubgenera have been considered less distinctfrom one another than have the other sub-genera of Bombus (Pittioni, 1939; Ito, 1985;Williams, 1985; Michener, 1990) and have


Figure 1. Recently listed bumblebee subgenera(e.g. Michener, 2000, 2007; divided into species-groups where necessary to recognise only strictlymonophyletic clades, some of which may consist ofa single species) showing the estimate of phylogenyredrawn from Cameron et al. (2007). Only cladeswith strong support (Bayesian posterior probability� 0.95) are shown.

been synonymised with a genus (Milliron,1961) or subgenus (Williams, 1991) Psithyrus.Some authors have preferred to continue touse these subgenera (e.g. Rasmont, 1983).But in recognition of the importance of themany morphological and behavioural homolo-gies among Psithyrus in the broad sense (e.g.Williams, 1995), more than for any other sin-gle clade, we agree that a single subgenusPsithyrus should be retained for the cuckoobumblebees. This has also gained widespreadacceptance and stability.

If Psithyrus is to remain as a single sub-genus, then from the best current estimate ofbumblebee phylogeny (Fig. 1), the minimumtotal number of subgenera required if all sub-genera were to be monophyletic would benine (Mendacibombus, Bombias, Kallobom-bus, Orientalibombus, Subterraneobombus,Megabombus, Thoracobombus, Psithyrus, anda large Bombus s. str.). Among these subgen-era, four are accepted here in the recent sensebecause they are then unavoidably requiredto maintain monophyly once Psithyrus is ac-cepted: Mendacibombus, Kallobombus, Ori-entalibombus, and Subterraneobombus. Theothers are discussed below.

Bombias: Bombias + Confusibombus. Thesubgenus Confusibombus has been seen pre-viously as part of a ‘section’ Bombias byKruseman (1952) (and the section Boopobom-bus Frison was synonymised with the sub-genus Bombias by Williams, 1995). Thepossible argument in favour of retaining a splitbetween them is that this represents an earlydivergence, dating to nearly half of the age ofthe inclusive Bombus clade (Hines, in press).Our argument in favour of lumping is that withso few species (three), uniting them within asingle subgenus Bombias is useful to empha-sise their unusual shared morphological char-acter states of both sexes, such as the combina-tion of male short antennae, large eyes, straightpenis valves, and gonostyli and volsellae withinner processes (see the keys in Appendices).

Megabombus: Diversobombus + Senexi-bombus + Megabombus. These subgenerahave been synonymised previously (Milliron,1961) (the ‘section’ Odontobombus Krügerhas also been synonymised with the subgenusMegabombus by Milliron, 1961, and Williams,


Figure 2. Proposed simplified bumblebee subgen-era showing the estimate of phylogeny redrawnfrom Cameron et al. (2007). Only clades withstrong support (Bayesian posterior probability �0.95) are shown. Three characters that are tradi-tionally associated with the group marked with thegrey box (Orientalibombus + Subterraneobombus+Megabombus + Thoracobombus + Psithyrus) aremapped against the tree using data from Table IIIand from Appendix 1 (‘?’ is used for unknown [Ori-entalibombus, Sibiricobombus] states and ‘X’ forunobservable [Psithyrus] states).

1995). Our argument in favour of treating thisclade as a single subgenus is that it recog-nises a group for many of the species with thelongest tongues among bumblebees.

Thoracobombus: Tricornibombus + Ex-ilobombus + Fervidobombus + Rhodobom-bus + Laesobombus + Eversmannibombus+ Mucidobombus + Thoracobombus. Thisvery large clade includes eight subgenera insome recent publications, although Laesobom-bus, Eversmannibombus and Mucidobom-bus have been synonymised previously withThoracobombus (Tkalcu, 1972; Reinig, 1981;Rasmont, 1983). The oldest available namesfor the large clade are Thoracobombus andRhodobombus, of which we choose Thora-

cobombus as the valid name by the princi-ple of the First Reviser (ICZN, 1999). DNAevidence shows that there are two weakly-supported similarly-sized subclades (Cameronet al., 2007: their Fig. 1), one predominantlyOld World and one predominantly New World.A few species of each of these two subclades(e.g. B. pascuorum and B. fervidus respec-tively) are well known from their respectiveregions, and these species give the impressionthat the two subclades are strongly distinct.However, some of the less well known speciesof each subclade show the character states ofthe sister clade (i.e. both subclades show sim-ilar broad ranges in characters such as aggres-siveness, colony size, nest position relative toground level) so that there is overlapping vari-ation between both subclades. In the DNA tree(Fig. 1), five subclades remain unresolved at abasal level in this large clade. Most of theseare currently morphologically undiagnosablein one or both sexes when all known speciesare examined. A few small subclades (e.g. theformer subgenus Rhodobombus) are easily di-agnosable from morphological characters, butrecognising these as separate subgenera wouldleave large paraphyletic subgenera. In addi-tion, former concepts of some subgenera (Fer-vidobombus, Tricornibombus) are recognisednow as polyphyletic. We have a precedent fora similarly large and diverse subgenus in thelong-accepted Pyrobombus.

In recent publications, the remaining bum-blebees include several medium to large, well-diagnosed subgenera and many small andpoorly-diagnosed subgenera. The first cate-gory consists of the subgenera Alpinobombus,Bombus (in the narrow sense), Pyrobombus,and Alpigenobombus, which we accept as sep-arate without change (the ‘section’ Anodon-tobombus Krüger was synonymised with thesubgenus Pyrobombus by Milliron, 1961, andWilliams, 1995). The one change to Pyrobom-bus (Cameron et al., 2007) is that the uniquelydivergent, single species of Pressibombus isnow recognised as a part of Pyrobombus. Ourargument in favour of maintaining the separa-tion of these four larger subgenera is that eachis distinctive and reasonably homogeneous inthe morphology of both sexes (see Appen-dices).


Melanobombus: Rufipedibombus + Fes-tivobombus + Melanobombus. Our argumentin favour of lumping these clades is that theyare morphologically similar in both sexes (seeAppendices).

Sibiricobombus: Sibiricobombus + Ober-tobombus. These subgenera have beensynonymised previously (Richards, 1968;Williams, 1991). Our argument in favourof lumping these clades is that they havevery long tongues (Williams, 1991) and areotherwise morphologically similar in bothsexes (see Appendices).

Cullumanobombus: Cullumanobombus +Brachycephalibombus + Rubicundobombus +Coccineobombus + Dasybombus + Crotchi-ibombus + Separatobombus + Funebribom-bus + Fraternobombus + Robustobombus. Inrecent publications, most of these subgen-era include just one or two species, althoughmany of the subgenera have been synonymisedpreviously by Milliron (1961). Two smallsubgroups are distinctive. The first subgroupincludes B. rufocinctus and the cullumanus-group, but this may or may not form a mono-phyletic clade (Cameron et al., 2007). Whereasmales of most species of Cullumanobombus inthe broad sense have eyes enlarged relative tothe females, males in this subgroup (of smallsteppe species) have their eyes relatively unen-larged. The second subclade includes B. han-dlirschi and the coccineus-group, which aremountain bumblebees, but which also haveless strongly enlarged male eyes. While thereis morphological heterogeneity in the largerinclusive clade, especially in the males, the fe-males are morphologically more similar.

Our proposed simplified subgeneric clas-sification is summarised with the phylogenyin Figure 2 and listed with the neces-sary nomenclatural changes in Table I.A full synonymic list of bumblebee sub-generic names with minor corrections fromSandhouse (1943), Richards (1968), Michener(1997, 2000, 2007), and Williams (1998) canbe found at <http://www.nhm.ac.uk/research-curation/projects/bombus/groups.html>. Thekeys were prepared from a survey of morpho-logical characters by mapping character-statechanges onto the molecular estimate of thephylogenetic tree in order to identify which

states diagnose subgenera or groups of sub-genera.

5. ASSESSMENT

We can assess the degree of success of theproposed subgeneric system (Fig. 2) in meet-ing each of the criteria listed above as follows:

Monophyly. All bumblebee subgenera inFigure 2 are monophyletic according tothe strongly supported published evidence(Cameron et al., 2007).

Fewer. The number of bumblebee subgen-era world-wide is reduced from 38 to 15. Theconsequences of this simplification for con-tinental counts of indigenous subgenera areshown in Table II.

Morphological diagnosability. Illustratedkeys for the identification of the bumblebeesubgenera from the morphological charactersof both sexes are included here (Appendices).Our tests show that, while many of the charac-ters are not as easy to use as we would wish,the diagnoses give correct subgeneric determi-nations for all but a few of the smallest speci-mens tested so far.

The keys include exceptions for the char-acters of a few early-diverging species withinthe enlarged subgenera Melanobombus, Sibiri-cobombus, and Cullumanobombus. Thesespecies could be recognised as separate sub-genera with the available names Rufipedi-bombus, Festivobombus, Obertobombus, Ru-focinctobombus, and Cullumanobombus (inthe narrow sense, which would then have to bedistinguished from an enlarged Robustobom-bus). However, several of these former subgen-era are undiagnosable by morphology in oneof the sexes. None is known to be particularlystrongly differentiated in behavioural or eco-logical characters. Consequently, at present wesee no substantial benefit in separating themfrom their larger sister groups in a series ofmonotypic or near-monotypic subgenera. Wesee greater benefit in recognising the broaderhomologies across the larger, more inclusivesubgenera.

Behavioural and ecological groups. Sub-genera in the simplified system can in many


Table I. Summary of nomenclature for the proposed simplified subgeneric system.

Proposed simplified No. of Synonyms amongsubgenera species* recent subgenera**

1 Mendacibombus Skorikov 122 Bombias Robertson 3

Confusibombus Ball syn. n.3 Kallobombus Dalla Torre 14 Orientalibombus Richards 35 Subterraneobombus Vogt 106 Megabombus Dalla Torre 22

Diversobombus SkorikovSenexibombus Frison

7 Thoracobombus Dalla Torre 50Eversmannibombus SkorikovExilobombus Skorikov syn. n.Fervidobombus Skorikov syn. n.Laesobombus KrügerMucidobombus KrügerRhodobombus Dalla Torre syn. n.Tricornibombus Skorikov syn. n.

8 Psithyrus Lepeletier 309 Pyrobombus Dalla Torre 50

Pressibombus Frison syn. n.10 Alpinobombus Skorikov 511 Bombus s. str. 1012 Alpigenobombus Skorikov 713 Melanobombus Dalla Torre 17

Festivobombus Tkalcu syn. n.Rufipedibombus Skorikov syn. n.

14 Sibiricobombus Vogt 7Obertobombus Reinig

15 Cullumanobombus Vogt 23Brachycephalibombus Williams syn. n.Coccineobombus SkorikovCrotchiibombus FranklinDasybombus Labougle & Ayala syn. n.Fraternobombus SkorikovFunebribombus SkorikovRobustobombus SkorikovRubicundobombus SkorikovSeparatobombus Frison

* Complete list of nomenclature and species at <http://www.nhm.ac.uk/research-curation/projects/bombus/groups.html>.** From the most recent published list in Michener (2000, 2007).

cases be associated with particular combi-nations of behavioural and ecological char-acter states (these are summarised crudelyin Table III, but published information isfar from adequate). For example, species ofMendacibombus and Bombias have distinc-

tive nest-building behaviour (Hobbs, 1965;Haas, 1976). Many (but not all) species ofMegabombus have the longest tongues amongbumblebees and specialise in visiting partic-ularly deep flowers, sometimes of very fewplant species (e.g. Løken, 1973). Species of


Table II. Geographical distribution of recent and proposed bumblebee subgenera.

Continent/region No. of species* Recent subgenera** Proposed simplified subgenera1 Western Palaearctic 72 18 142 Eastern Palaearctic 96 20 143 Oriental 108 19 114 Nearctic 58 14 85 Neotropical 25 7 3

* From the list of species at <http://www.nhm.ac.uk/research-curation/projects/bombus/groups.html>.** From the most recent published list in Michener (2000, 2007).

Thoracobombus in the new broad sense (bothOld World and New World) often have mod-erately long tongues and include all of thespecies described by Sladen (1912) as ‘carderbees’. Many of these species build nests onthe surface of the ground, covered only byherbaceous plant material, such as grass stems(broadly similar behaviour is also known forsome of the South American tropical lowlandforest species, e.g. Cameron and Whitfield,1996; other species build nests underground).Although social parasitism occurs elsewherein the genus, Psithyrus species are very dis-tinctive for their particular kind of parasiticbehaviour (e.g. Sladen, 1912). Alpinobombusspecies are well known for being specialistsin high arctic (and a few alpine) environments(e.g. Richards, 1973). Bombus s. str. speciesare regarded as having a distinctive social bi-ology that makes them particularly well suitedto management for pollination (e.g. Winteret al., 2006). Pyrobombus is a large and diverseclade, but includes many small species withshort colony cycles and which forage particu-larly often from hanging flowers (Prys-Jonesand Corbet, 1987). Alpigenobombus speciesare distinctive for having six large triangu-lar teeth on each mandible and for habitu-ally using them to bite through flower corol-las to rob nectar (e.g. Løken, 1973; Williams,1991). Melanobombus species are predom-inantly mountain bees (Williams, 1991; al-though the best known species, the EuropeanB. lapidarius and B. sichelii, are exceptionalfor being widespread in the lowlands in largeparts of their ranges) that nest underground,and at least in some cases, have a preferencefor composite inflorescences. Sibiricobom-bus species are steppe and mountain bees

with unusually long tongues (Williams, 1991;Rasmont et al., 2005). Cullumanobombusspecies are predominantly mountain species,although there are a few lowland species.

Combining former subgenera brings to-gether species with similar characteristics, sothat generally intra-subgeneric variation ap-pears to be less than inter-subgeneric vari-ation. A few small clades (e.g. the pomo-rum-group within Thoracobombus and someof the rufofasciatus-group within Melanobom-bus) are divergent, particularly in morphologi-cal characters relating to male mate-searchingbehaviour (e.g. Terzo et al., 2005, 2007a, b,and Williams, 1991: his Fig. 10, respectively).However, recognising these as separate sub-genera would leave large paraphyletic subgen-era. We consider that it is premature to attempta more quantitative assessment of behaviouraland ecological data at present because: (1) dataare available from relatively few species, witha strong bias towards those from north-westernEurope and from North America (Sakagami,1976); (2) character states have not been de-fined in a consistent manner in the literature(Sakagami, 1976); and (3) characters are of-ten variable within species and may dependupon environmental influences in ways thatare not yet fully understood (Sakagami, 1976;Plowright, 1977).

There would be potential pitfalls in pursu-ing simplification of the subgeneric system toofar. If we exclude from this discussion the par-asitic species of the subgenus Psithyrus, thenmany authors (often faced with restricted re-gional faunas) have regarded the remainingsocial bumblebees as being divided into twobroad groups. However, Figure 2 shows thatdifferent versions of the two groups based on

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each of three popular characters are not mono-phyletic, even if the early-diverging subgeneraMendacibombus, Bombias, and Kallobombus(Fig. 2) were also excluded from considera-tion. First, Sladen’s (1912) group of ‘pocketmakers’ is now known to include not onlythe subgenera Subterraneobombus, Megabom-bus, and Thoracobombus, as originally de-scribed, but also Alpinobombus, Alpigenobom-bus, and Cullumanobombus, at least as faras the early stages of nest development areconcerned (Fig. 2). Second, Krüger’s (1917)group of bumblebees with a spine on themid basitarsus (his ‘section’ Odontobombus),which excited much interest because it wasseen as being associated with Sladen’s originalgroup of pocket makers (Subterraneobombus,Megabombus, and Thoracobombus), also in-cludes Alpigenobombus and Sibiricobombus,but excludes Orientalibombus, Alpinobom-bus and Cullumanobombus (Fig. 2). Third,tongue length (e.g. Medler, 1962), which isso important for governing food-plant prefer-ences (e.g. Harder, 1983), is not only long aswidely recognised (e.g. Kawakita et al., 2004;Cameron et al., 2007) for the group of sub-genera Orientalibombus, Subterraneobom-bus, Megabombus, and some Thoracobombus,but is also long for a few Melanobombus, someAlpinobombus, and is characteristically longfor Sibiricobombus (Fig. 2). As long ago as1977, Plowright (1977) cast doubt on the sup-posed association between the two major tax-onomic divisions of Krüger (1917) on the onehand and the two traditional groups of bum-blebees by brood-rearing behaviour (Sladen,1912) on the other.

In summary, we find that while it is straight-forward to recognise monophyletic subgeneraand to reduce their number, it is more diffi-cult to choose clades that are either easily di-agnosed morphologically, or clades that shareimportant behavioural and ecological charac-ters. In part this may be because ‘the [mor-phological] homogeneity of the species in thegenus is outstanding’ (Michener, 2000, 2007).But from Figure 2, it also appears that theremay be substantial homoplasy in behaviouralcharacters. We consider that the proposed sim-plified subgenera reflect the pattern of varia-tion in these characters more closely than re-

cent subgeneric systems. What is needed nowis to collect information on these characters ina consistent way and from many more speciesso that they can be mapped onto the phyloge-netic tree more precisely in order to clarify thisrelationship.

ACKNOWLEDGEMENTS

Our thanks to R. Thorp and an anonymous ref-eree for comments on the manuscript and to T.Benton, J. Cane, S. Corbet, S. Colla, L. Day, M.Edwards, D. Goulson, D. Inouye, L. Manne, J. Os-borne, L. Packer, J. Thomson, R. Thorp, R. Vane-Wright, and J. Whitfield for discussion. P. Williamsthanks E. Floess, J. Grixti, C. Rasmussen, and J.Whitfield for comments on the keys. Many SEMimages of female bumblebees were kindly pro-vided by M. Terzo and photomontage images ofmale genitalia were made by A. Polaszek. Ourthanks to the Swedish Species Information Cen-tre, Sveriges Lantbruksuniversitet, for supporting aworkshop in Uppsala (August 2006). S. Cameronand H. Hines were supported by USDA grants toSC (NRI, CSREES 2002-35302-11553 and 2004-35302-15077). P. Rasmant thanks Fonds Nationalde la Recherche Scientifique and the Fonds de laRecherche Fondamentale et Collective for supportfor preparing the bumblebee images.

Classification simplifiée des sous-genres de bour-dons (genre Bombus).

Bombus / sous-genre / phylogénie / classification

Zusammenfassung – Eine vereinfachte Klassifi-kation der Untergattungen der Hummeln (Gat-tung Bombus). Hummeln sind farblich sehr varia-bel, morphologisch ansonsten aber relativ einheit-lich. Um die Variation sinnvoll zu ordnen, bestehteine lange Tradition die Arten in Untergattungenzusammenzufassen und sich hierbei zunächst aufdie Färbung, dann auf die Morphologie und neu-erdings auch auf DNA Sequenzen zu stützen. Al-lerdings wurde bei 38 Unterarten in den derzeitigenListungen die Notwendigkeit einer Vereinfachungdes Systems gesehen. Wir besprechen die weiter-hin bestehende Nützlichkeit des Systems von Un-tergattungen und erörtern vier mögliche als Leitli-nie für Änderungen nutzbare Kriterien. Wir schla-gen vor, dass Untergattungen (1) monophyletisch,(2) weniger, (3) aus der Morphologie erkennbarwerden sollten und (4) zur Namensgebung wichti-ger verhaltensmäßiger oder ökologischer Gruppen


dienlich sein sollten. Unter Nutzung einer fast alleHummeln einschließenden gut fundierten Abschät-zung der Phylogenie besprechen wir Konflikte inder Nutzung dieser Kriterien und schlagen ein ver-einfachtes System aus 15 Untergattungen vor, in der10 neue Untergattungssynonyme anerkannt werden.Wir fanden es leicht, monophyletische Subgenerazu erkennen und ihre Anzahl zu reduzieren. Dage-gen wurde es mit zunehmender Artenzahl immerschwieriger, Untergattungen zu definieren, die so-wohl morphologisch leicht zu unterscheiden warenals auch einige der oft als besonders wichtig ange-sehenen verhaltensmässigen und ökologischen Ei-genschaften teilen. Dies war deshalb der Fall, daentsprechend unserer vorläufigen Analyse einzel-ne Ausprägungen dieser Eigenschaften nicht aus-schließlich von allen Arten einer morphologischenGruppe geteilt werden.

Hummeln / Bombus / Untergattungen / Phyloge-nie / Klassifikation

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Williams P.H. (1995) Phylogenetic relationshipsamong bumble bees (Bombus Latr.): a reappraisalof morphological evidence, Syst. Entomol. 19,327–344.

Williams P.H. (1998) An annotated checklist ofbumble bees with an analysis of patterns of de-scription (Hymenoptera: Apidae, Bombini), Bull.

Nat. Hist. Mus. Lond. (Entomol.) 67, 79–152,[updated at <http://www.nhm.ac.uk/research-curation/projects/bombus/>].

Winter K., Adams L., Thorp R.W., Inouye D.W., DayL., Ascher J., Buchmann S. (2006) Importation ofnon-native bumble bees into North America: po-tential consequences of using Bombus terrestrisand other non-native bumble bees for green-house crop pollination in Canada, Mexico, andthe United States, p. 33, A White Paper of theNorth American Pollinator Protection Campaign(NAPCC).

APPENDIX 1

Key to simplified subgenera of the genusBombus for female bumblebees

Paul H. Williams

With SEM images by Michael Terzo, PierreRasmont, Paul Williams.

The keys have been simplified as far aspossible to make them easier to use. Keyswill generally be easier to use for largerand younger (less worn) individuals, and ifthey have had their mandibles opened andare cleaned of debris. Differences in the mid-basitarsal spine and face length are clearer forlarger individuals and may be relatively undif-ferentiated for smaller individuals.

1 Hind tibia with the outer surface broad,almost flat, most of the outer surface in thedistal half without moderate to long hairs(Fig. 3a arrow), but fringed with stout hairsthat form a pollen basket (corbicula), theinner distal margin with a comb of stoutspines (rastellum); gastral sternum 6 withoutventro-lateral keels . . . . . . . . . . . . . . . . . . . . . . . 2

- Hind tibia with the outer surface stronglyand uniformly convex and uniformly denselycovered with moderate to long stout hairsthroughout (Fig. 3b arrow), the fringing hairsoften poorly differentiated and not forming apollen basket (corbicula), the inner distal mar-gin without a comb of stout spines (rastellum);gastral sternum 6 with ventro-lateral keels(Fig. 4 arrow). (Holarctic, Oriental) Psithyrus


3a 3b 3c

5d

3c

4 5a 5b 5c

7b6a 7a6b

8a 8b

Figures 3–8. 3: Female left hind tibia from the outer lateral aspect for (a) B. (Pr.) pratorum; (b) B. (Ps.)campestris; (c) B. (Md.) avinoviellus. 4: Female sternum 6 from the ventral aspect for B. (Ps.) moraw-itzianus. 5: Female left mandible from the outer lateral aspect for (a) B. (Ml.) rufofasciatus; (b) B. (Md.)avinoviellus; (c) B. (Ml.) rufofasciatus; (d) B. (Ag.) kashmirensis. 6: Female left hind tibia from the outerlateral aspect for (a) B. (Pr.) subtypicus; (b) B. (Md.) avinoviellus. 7: Female left mid basitarsus from theouter lateral aspect for (a) B. (Mg.) trifasciatus; (b) B. (Or.) haemorrhoidalis. 8: Female proximal third ofthe left hind basitarsus from the outer lateral aspect of (a) B. (Ml.) semenovianus; (b) B. (Sb.) oberti. Forall figures, anterior is towards the left of the page and posterior is towards the right. For explanations of thearrows and circles, see the text.


9a 9b

9e 9f

9c 9d

10a

10c 10d 10e 10f

10b

Figures 9–10. 9: Left half of the female head from the anterio-dorsal aspect of (a) B. (Th.) pomorum;(b) B. (Sb.) niveatus; (c) B. (Pr.) pratorum; (d) B. (Or.) haemorrhoidalis; (e) B. (Pr.) pratorum; (f) B. (Kl.)soroeensis. 10: Left ventral part of the female head from the anterio-lateral aspect of (a) B. (Th.) pascuorum;(b) B. (St.) subterraneus; (c) B. (Bo.) terrestris; (d) B. (Cu.) cullumanus appolineus; (e) B. (Cu.) cullumanusappolineus; (f) B. (Kl.) soroeensis. For all figures, anterior is towards the left of the page and posterior istowards the right. For explanations of the lines and circles, see the text.


2 (1) Mandible with the anterior keel reach-ing and continuous with the distal margin(Fig. 5a circled); hind basitarsus with theproximal posteriorly-directed process usuallynarrow and pointed, longer than its breadthproximally where it joins the basitarsus(Fig. 6a lines), or if it is shorter than broadthen either the lateral ocellus diameter equal tohalf or less than half of the distance separatingthe lateral ocellus from the inner margin ofthe eye (e.g. some of the hypnorum-groupof Pyrobombus and some Melanobombus,from the Palaearctic and Oriental), or thehair on the side of tergum 2 is longer thanthe breadth of the hind basitarsus and thelabrum has a strong longitudinal medianfurrow and ventral transverse lamella (therare parasitic B. (Th.) inexspectatus, from theAlps), or the hind basitarsus narrows distallyto 0.66–0.75 times the proximal breadthjust distal to the proximal process (B. (Cu.)rubicundus and B. (Cu.) handlirschi, from theAndes) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

- Mandible with the anterior keel notreaching and separated from the distal margin(Fig. 5b circled); hind basitarsus with theproximal posteriorly-directed process broadand blunt, usually shorter than its breadthproximally where it joins the basitarsus(Fig. 6b lines); lateral ocellus diameter alwaysnearly three quarters or more of the distanceseparating the lateral ocellus from the innermargin of the eye; either the hair on theside of tergum 2 is shorter than half of thebreadth of the hind basitarsus, or the labrumlacks a distinct longitudinal median furrowand ventral transverse lamella, or both; hindbasitarsus nearly equal in breadth distally andproximally beyond the proximal process . . . . 3

3 (2) Hind tibia with the outer surfacecoarsely sculptured (imbricate), matt andnot shining, with very long stout hairs inthe middle of the proximal half that arespaced widely by more than the breadthof an antennal segment (Fig. 3c arrow).(Palaearctic) . . . . . . . . . . . . . . .Mendacibombus

- Hind tibia with the outer surface weaklysculptured (reticulate coriaceous), smooth and

brightly shining, and without long stout hairsin the middle of the proximal half beyond theproximal quarter (similar to Fig. 3a arrow).(Holarctic) . . . . . . . . . . . . . . . . . . . . . . . Bombias

4 (2) Mandible distally broadly rounded,with two anterior teeth and often a posteriortooth (Fig. 5c spots); hind basitarsus with thelongest erect hairs near the anterior margin ofthe outer surface shorter than the narrowestbreadth of the basitarsus . . . . . . . . . . . . . . . . . . 5

- Mandible distally not broadly rounded,but with six evenly-spaced large triangu-lar teeth (which may become worn down)(Fig. 5d spots); hind basitarsus with thelongest erect hairs near the anterior marginof the outer surface as long or longer thanthe narrowest breadth of the basitarsus (butwhich may become broken off). (Palaearctic,Oriental) . . . . . . . . . . . . . . . . . .Alpigenobombus

5 (4) Mid basitarsus with the distal pos-terior corner extended to form a sharp angleof 45◦ or less, often produced as a narrowtooth or spine (Fig. 7a lines) (it may be lesspronounced in some of the smallest individ-uals), or if borderline then the ocello-oculararea with the unpunctured and shining areasoccupying less than half of the distancebetween the lateral ocellus and the innermargin of the eye (e.g. B. (Th.) digressus,from Central America, and B. (Sb.) sibiricus,from the eastern Palaearctic and Oriental).(Note: oculo-malar distance approximately1.0–2.5 times the breadth of the mandibleproximally between the outer ends of itsarticulations [condyles].) . . . . . . . . . . . . . . . . . . 6

- Mid basitarsus with the distal posteriorcorner broadly or narrowly rounded, but form-ing an angle of more than 45◦, and withouta narrow tooth or spine (Fig. 7b lines), orif borderline then the ocello-ocular area withthe unpunctured and shining areas occupyingthree quarters of the distance between the lat-eral ocellus and the inner margin of the eye(e.g. B. (Pr.) hypnorum, from the Palaearcticand Oriental). (Note: oculo-malar distance ap-proximately 0.5–1.6 times the breadth of the


10g

11a 11b 11c 11d

10h

Figures 10–11. 10: Left ventral part of the female head from the anterio-lateral aspect of (g) B. (Cu.)cullumanus appolineus; (h) B. (Kl.) soroeensis. 11: Female left mandible from outer lateral aspect of (a) B.(Bo.) terrestris; (b) B. (Kl.) soroeensis; (c) B. (Kl.) soroeensis; (d) B. (Cu.) cullumanus appolineus. For allfigures, anterior is towards the left of the page and posterior is towards the right. For explanations of thearrows and circles, see the text.

mandible proximally between the outer endsof its articulations [condyles].) . . . . . . . . . . . . 9

6 (5) Hind basitarsus with the proximalposteriorly-directed process with the denseplume of moderately long branched hairs on itsproximal surface not continuing onto its outersurface, which is shining and often bare, or atmost the outer surface with widely scatteredrather decumbent short hairs with broad shin-ing areas between them (Fig. 8a circled); me-dian ocellus with its anterior margin lying ona line linking the corners between the ante-rior and dorsal margins of each compound eye(Fig. 9a line) . . . . . . . . . . . . . . . . . . . . . . . . . . . . .7

- Hind basitarsus with the proximalposteriorly-directed process with the denseplume of moderately long branched hairson its proximal surface continuing ontoits outer surface as a dense erect brush ofmoderately long branched hairs that obscuresthe outer surface of the basitarsus betweenthem (Fig. 8b circled); median ocellus with itsanterior margin lying anterior to a line linkingthe corners between the anterior and dorsalmargins of each compound eye (Fig. 9b line).(Palaearctic, Oriental) . . . . . . . Sibiricobombus

7 (6) Clypeus with scattered large mediumor small punctures over most of its area


(Fig. 10a circled), or at least extending ontothe outer quarters of the weakly flattened,bulbous, central area (e.g. B. (Mg.) hortorum,from the Palaearctic), or forming very densepatches in the lateral depressions adjacent andparallel to the ventral labral margin (e.g. B.(Mg.) senex, from Sumatra); if the corbicularfringes are shorter than the greatest breadthof the hind tibia then the proximal half ofthe outer surface of the hind tibia has longhairs in the centre (and the body hair is allblack: B. (Th.) brevivillus, from north-easternBrazil); sternum 6 without a raised medianlongitudinal ridge in the posterior one third,or if a strong ridge is present then either theclypeus has medium and large punctures (e.g.B. (Th.) muscorum, from the Palaearctic) orantennal segment 4 is shorter than broad (e.g.B. (Mg.) trifasciatus, from the Oriental) . . . . 8

- Clypeus predominantly smooth andshining, the strongly flattened central areawith only widely scattered micro-punctures(Fig. 10b circled), larger punctures only atthe edges, or if more extensively coveredwith many small and medium punctures thenthe corbicular fringes are shorter than thegreatest breadth of the hind tibia and theproximal half of the outer surface of the hindtibia has no long hairs in the centre beyondthe proximal quarter (and the dorsal bodyhair is extensively yellow: B. fragrans, B.fedtschenkoi, and B. amurensis, from the cen-tral and eastern Palaearctic); sternum 6 witha raised and often shiny median longitudinalkeel in the posterior one third. (Holarctic,Oriental) . . . . . . . . . . . . . . Subterraneobombus

8 (7) Sternum 2 usually slightly bulgingbetween the anterior and posterior margins ina weak rounded transverse ridge; hind tibiawith the corbicular surface at least moderatelyconvex anteriorly and often swollen andalmost lacking any posterior concavity in thedistal half, or if flatter then either the clypeusis densely punctured (e.g. dahlbomii-group,from the Neotropics), or the ocello-oculararea with the unpunctured and shining areasoccupying two thirds of the distance betweenthe lateral ocellus and the inner margin of theeye (e.g. B. pomorum, from the Palaearctic);

clypeus dorsally uniformly convex and alwayswithout a deep dorsal median longitudinalgroove with many punctures, clypeus in itscentral half with a few large punctures andsometimes densely punctured, or if it hasonly sparsely scattered fine punctures thenthere is no dorsal groove and the dorsalthoracic hair is largely orange-brown andsegment 4 of the antenna is longer than broad(e.g. B. pascuorum, from the Palaearctic).(Note: oculo-malar distance approximately1.0–1.5 times the breadth of the mandibleproximally between the outer ends of itsarticulations [condyles].) (Holarctic, Oriental,Neotropics) . . . . . . . . . . . . . . . .Thoracobombus

- Sternum 2 flat between the anterior andposterior margins, with the weakly bulgingtransverse ridge absent; hind tibia withthe corbicular surface nearly flat and onlyvery weakly convex anteriorly and concaveposteriorly in the distal half; clypeus inits dorsal third often with a deep medianlongitudinal groove with many punctures(supremus-consobrinus-group), clypeus inits central half shining with only sparselyscattered small punctures and no large ordense punctures. (Note: oculo-malar distanceapproximately 1.0–2.5 times the breadth of themandible proximally between the outer endsof its articulations [condyles].) (Palaearctic,Oriental) . . . . . . . . . . . . . . . . . . . . . Megabombus

9 (5) Ocello-ocular area with the unpunc-tured and shining areas medium or small, thearea anterior to the three ocelli unpuncturedfor less than the breadth of an ocellus (Fig. 9cbox), or if this area is largely unpuncturedthen the diameter of the lateral ocellus is morethan half of the distance separating the lateralocellus from the inner margin of the eye(e.g. B. (Cu.) brachycephalus, from CentralAmerica) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

- Ocello-ocular area with the unpuncturedand shining areas very large and includingmost of the area anterior to the three ocellifor a distance of more than the breadth of anocellus except for narrow bands of puncturesbetween the median and lateral ocelli (Fig. 9dbox); diameter of the lateral ocellus less than


or equal to half of the distance separating thelateral ocellus from the inner margin of theeye. (Oriental) . . . . . . . . . . . . .Orientalibombus

10 (9) Mandible distally with a notch(incisura) nearly as deep as wide (Fig. 11aarrow) separating a strong posterior tooth(which may become worn down); clypeusin the dorsal half always strongly swollenand bulging, concave ventrally with deeplateral depressions adjacent and parallel tothe labral margin (Fig. 10c); diameter of thelateral ocellus less than or equal to half ofthe distance separating the lateral ocellus fromthe inner margin of the eye; labrum alwayswith a broad median longitudinal furrow; hindtibia outer surface in the proximal half withoutlong hairs beyond the proximal quarter . . . . 11

- Mandible distally with a notch (incisura)less than half as deep as wide, or oftencompletely lacking (Fig. 11b arrow) and notseparating a weak posterior tooth; clypeususually weakly swollen or nearly flat through-out, with only shallow lateral depressionsadjacent and parallel to the ventral labralmargin (Fig. 10d), or if it is strongly swollendorsally and concave ventrally then eitherthe diameter of the lateral ocellus is morethan half of the distance separating the lateralocellus from the inner margin of the eye(e.g. B. (Cu.) brachycephalus, from CentralAmerica), or the labrum has almost no medianlongitudinal furrow and the hind tibia has theouter surface in its proximal half with longhairs throughout (B. (Cu.) rubicundus, fromthe Andes) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

11 (10) Hind basitarsus with the pos-terior margin strongly and evenly convex;oculo-malar distance just shorter or dis-tinctly shorter than the breadth of themandible proximally between the outer endsof its articulations (condyles). (Holarctic,Oriental) . . . . . . . . . . . . . . . . . . . . Bombus s. str.

- Hind basitarsus with the posteriormargin strongly convex in its proximalquarter, the remainder nearly straight; oculo-malar distance longer than the breadthof the mandible proximally between the

outer ends of its articulations (condyles).(Holarctic) . . . . . . . . . . . . . . . . . . Alpinobombus

12 (10) Median ocellus with its anteriormargin lying on a line linking the cornersbetween the anterior and dorsal margins ofeach compound eye (similar to Fig. 9a line),the diameter of the lateral ocellus less thanhalf or equal to half of the distance separatingthe lateral ocellus from the inner margin ofthe eye, or if the ocelli are larger and situatedmore anteriorly then the hind basitarsus hasvery densely overlapping pale short plumosehairs throughout the outer surface excludingthe proximal posterior process (B. (Ml.)rufofasciatus and B. (Ml.) simillimus, from theHimalaya); hind basitarsus with the posteriormargin convex in the proximal quarter, theremainder nearly straight, or if it is moreevenly convex then this is weak and nearlystraight (e.g. B. (Kl.) soroeensis, from thePalaearctic); mandible with the posteriorgroove (sulcus obliquus) indistinct or absent(Fig. 11c circled), or if stronger then again thehind basitarsus has very densely overlappingpale yellowish short plumose hairs throughoutits outer surface excluding the proximalposterior process (e.g. B. (Ml.) lapidarius,from Europe); oculo-malar distance nearly aslong as (0.9 times) or longer than the breadthof the mandible proximally between the outerends of its articulations (condyles) . . . . . . . . 13

- Median ocellus with its anterior margin ly-ing anterior to a line linking the corners be-tween the anterior and dorsal margins of eachcompound eye (similar to Fig. 9b line), the di-ameter of the lateral ocellus more than half ofthe distance separating the lateral ocellus fromthe inner margin of the eye, or if the ocelli aresmaller then the hind basitarsus has the pos-terior margin strongly and nearly evenly con-vex (cullumanus-group, from the Palaearctic);mandible with the posterior groove (sulcusobliquus) present (Fig. 11d circled); if the hindbasitarsus on its outer surface has pale yel-lowish short plumose hairs, then they are notdensely overlapping, at least in the proximalquarter; oculo-malar distance either equal to(e.g. B. coccineus, from the Andes) but may bemuch shorter than (0.5–1.0 times) the breadth


of the mandible proximally between the outerends of its articulations (condyles). (Holarctic,Neotropics) . . . . . . . . . . . . . Cullumanobombus

13 (12) Ocello-ocular area with the bandof punctures along the inner margin of theeye almost always with very few small punc-tures, only scattered large punctures separatedby more than their own widths (Fig. 9e cir-cled), the unpunctured and shining areas usu-ally large, occupying as much as three quar-ters of the distance between the lateral ocellusand the inner margin of the eye, or rarely theocello-ocular area almost completely coveredwith very dense intermediate-sized punctures(B. abnormis and B. mirus, from the centralHimalaya). (Holarctic, Oriental, northern edgeof the Neotropics) . . . . . . . . . . . . . Pyrobombus

- Ocello-ocular area with the band of punc-tures along the inner margin of the eye al-ways with many small and large punctures in-termixed and separated by less than the widthsof the large punctures (Fig. 9f circled), the un-punctured and shining areas occupying abouthalf of the distance between the lateral ocellusand the inner margin of the eye . . . . . . . . . . . 14

14 (13) Mid basitarsus with the longesterect hairs (which may become broken off)near the proximal margin of the outer surfacefrom the posterior aspect as long as or longerthan the distal breadth of the basitarsus, or ifshorter then the hind tibia with the distal poste-rior corner extended into a finger-like processthat is longer than broad (B. festivus, from theOriental); labrum with the median longitudinalfurrow broad, approximately one third of thetotal breadth of the labrum (similar to Fig. 10eline); clypeus shining with only widely scat-tered and mostly fine punctures (similar toFig. 10g circled), or if there is a clearer medianventral area then it is not narrowly raised; hindtibia with the outer corbicular surface some-times with short or medium hairs, but any longhairs are restricted to the proximal quarter or tothe outer edges. (Note: body length 9–32 mm.)(Palaearctic, Oriental) . . . . . . . Melanobombus

- Mid basitarsus with the longest erect hairsnear the proximal margin of the outer surfacefrom the posterior aspect shorter than thedistal breadth of the basitarsus; hind tibia withthe distal posterior corner scarcely extendedinto a finger-like process, which is shorter thanbroad; labrum with the median longitudinalfurrow narrow, approximately one fifth of thetotal breadth of the labrum (Fig. 10f line);clypeus in the central area densely coveredwith large and small punctures, except ina slightly narrowly raised ventral medianlongitudinal band which is unpunctured andshiny (Fig. 10h circled); hind tibia with theouter corbicular surface without short ormedium hairs but sometimes with one or twoscattered long stout hairs near the centre in theproximal half. (Note: body length 9–18 mm.)(Palaearctic) . . . . . . . . . . . . . . . . . . Kallobombus

APPENDIX 2

Key to simplified subgenera of the genusBombus for male bumblebees

Paul H. Williams

With photomontage images by Andrew Po-laszek.

This key is based largely on morphologicalcharacters of the male genitalia (parts labelledin Fig. 12), because these characters are morereliable and more clearly distinctive than othermorphological characters.

1 Gonostylus with the inner proximalprocess without medium-length branchedhairs (Fig. 13a arrow); volsella and gonostylususually strongly sclerotised and mid or darkbrown in colour; volsella often but not alwayswith a process or hooks on its inner margin;penis valve head either straight, or curvedinwards, or curved outwards . . . . . . . . . . . . . . .2

- Gonostylus with the inner proximalprocess associated with many medium-lengthbranched hairs (Fig. 13b arrow); volsellaand gonostylus usually weakly sclerotisedand pale yellowish in colour; volsella always


without a process or hooks on its inner mar-gin; penis valve head always nearly straight.(Holarctic, Oriental) . . . . . . . . . . . . . . Psithyrus

2 (1) Antenna medium to long, reachingback at least to the anterior margin of thetegula at the wing base; penis spatha narrowlyand sharply pointed at its proximal end(Fig. 14a circled), or if rounded then thespatha is broader than long (B. (Th.) digressus,from Central America); penis valve headeither straight, or curved inwards, or curvedoutwards; eye either enlarged or not enlargedrelative to the females . . . . . . . . . . . . . . . . . . . . 4

- Antenna short, not quite reaching back tothe anterior margin of the tegula at the wingbase; penis spatha rounded at its proximal end(Fig. 14b circled); penis valve head alwaysstraight; eye always strongly enlarged relativeto the females . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

3 (2) Volsella without a process or hookon its inner margin (Fig. 13c circled); volsellawith long hairs on its outer distal margin butno hairs on its inner distal margin (Fig. 13farrows); gonostylus simple and finger-like,without an inner proximal process, at mostwith a broad low proximal swelling (Fig. 13hcircled). (Palaearctic) . . . . . . .Mendacibombus

- Volsella with a process or hook onits inner margin, either near the mid pointof its length (Fig. 13d circled) or near itsdistal end (Fig. 13e circled); volsella withonly short hairs on its outer and inner distalmargins (Fig. 13g arrows); gonostylus eitherwith an inner proximal process (Fig. 13icircled), or divided into dorso-ventraland horizontal lamellae (Fig. 13j arrows).(Holarctic) . . . . . . . . . . . . . . . . . . . . . . . Bombias

4 (2) Penis valve narrow dorso-ventrally,at least in its distal third, which is slightlyventrally curved (Fig. 15a between the lines);antenna either of medium length or longer,reaching to or beyond the tegula at the wingbase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

- Penis valve greatly broadened dorso-ventrally so as to form half of a broad tube

(Fig. 15b between the lines), the distal endflared outwards as half of a broad funnel(Fig. 14c within the oval); antenna of mediumlength, not reaching back as far as the posteriormargin of the tegula at the wing base. (Holarc-tic, Oriental) . . . . . . . . . . . . . . . . . . . . Bombus s.str.

5 (4) Penis valve head from the dorsal as-pect turned inwards distally as a distinct broadhook, either dorso-ventrally flattened in theform of a sickle (Fig. 16a circled), or as an in-curved spoon (Fig. 16b circled), or if the hookis strongly reduced (Fig. 19a circled) then thepenis valve shaft has the ventral angle near itsmid-point absent (similar to Fig. 15c arrow) al-though there is still a ventral rounded angle atthe proximal end of the penis valve head (B.(Cu.) funebris and B. (Cu.) rubicundus, fromthe Andes) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

- Penis valve head from the dorsal aspectdistally either nearly straight (Fig. 16c circled)or turned slightly outwards (Fig. 16d circled),at most with only a tiny inwardly curved nar-row point . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

6 (5) Gonostylus with a distinct inner prox-imal process separate from the distal lobe(Fig. 13l circled), or if there is only one lobeor process then either it is reduced to a freelyarticulating transverse curved inner spine-likeplate and the gonocoxa has the inner distal cor-ner extended as a finger-like process that ismore than twice as long as broad (B. (Th.) im-itator, from southern China), or the gonocoxajust before the distal margin has a deep ovalsharply-defined mid-dorsal concavity and thespatha is nearly twice as broad as long (B. (Th.)digressus, from Central America) . . . . . . . . . . 7

- Gonostylus without a narrow inner proxi-mal process (Fig. 13k circled), at most markedwith a broad shallow curve or swelling, or ifthere is a very small sharp inner tooth thenthe distal lobe has a submarginal longitudinalgroove (Alpinobombus); gonocoxa with the in-ner distal corner rounded and just before itsdistal margin convex without a mid-dorsal ovalconcavity; spatha longer than broad . . . . . . . . 8


12

13a 13b

13c 13d 13e

13f 13g

Figures 12–13(a–g). 12: Male genital capsule from the dorsal aspect for B. (Md.) avinoviellus. 13: Maleleft gonostylus from the dorsal aspect for (a) B. (Th.) impetuosus; (b) B. (Ps.) citrinus; (c, f) B. (Md.)avinoviellus; (d, g) B. (Bi.) confusus; (e) B. (Bi.) auricomus. For all figures, anterior is towards the bottomof the page and posterior is towards the top. For explanations of the arrows and circles, see the text.


13h 13i

13k 13l

13j

13m 13n 13o

13p 13q

Figure 13(h–q). 13: Male left gonostylus from the dorsal aspect for (m, p) B. (Th.) impetuosus; (h) B. (Md.)avinoviellus; (j) B. (Bi.) confusus; (i) B. (Bi.) auricomus; (k) B. (Or.) haemorrhoidalis; (l) B. (Sb.) asiaticus;(n) B. (Th.) mexicanus; (o, q) B. (Mg.) koreanus. For all figures, anterior is towards the bottom of the pageand posterior is towards the top. For explanations of the arrows and circles, see the text.


13r 13s

13t 13u

13v 13w

13x 13y 13z 13aa

Figures 13(r–aa). 13: Male left gonostylus from the dorsal aspect for (u, w) B. (Or.) haemorrhoidalis; (r, t,v) B. (Kl.) soroeensis; (s) B. (Al.) alpinus.; (x) B. (Pr.) flavifrons; (y) B. (Pr.) pressus; (z) B. (Cu.) macgregori;(aa) B. (Cu.) handlirschi. For all figures, anterior is towards the bottom of the page and posterior is towardsthe top. For explanations of the arrows and circles, see the text.


7 (6) Volsella in ventral aspect in its distalhalf broad, the inner hooks (absent in B. per-sicus, from Turkey and Iran) placed eitherclose to the midpoint of its length between itsbroadest point and the distal end (Fig. 13mcircled), or if close to the distal end thenreduced to a broad blunt process (Fig. 13ncircled); gonostylus with the inner proximalprocess often weakly sclerotised in the ventralpart of the shelf, and if it has a long spinethen this is usually nearly straight, sharp andinwardly pointed (Fig. 13p circled); hind tibiawith the outer surface inside the posteriormargin convex, or if concave then the penisvalve head has an outer proximal hook thatis longer than the breadth of the adjacentpenis valve head (B. dahlbomii and B. morio,from South America). (Holarctic, Oriental,Neotropics) . . . . . . . . . . . . . . . .Thoracobombus

- Volsella in ventral aspect in its distalhalf narrow, the inner hooks pointed andalways placed close to the distal end (Fig. 13ocircled); gonostylus with the inner proximalprocess uniformly strongly sclerotised andstrongly re-curved away from the bodymidline and back towards the distal part ofthe gonostylus, with either at least one longstrongly curved tubular spine with a blunttip or flatter and with many teeth (Fig. 13qcircled); hind tibia with the outer surfaceinside the posterior margin concave, or ifconvex then the volsella has the more prox-imal of the inner hooks with many radiatingteeth (diversus-group, from eastern Asia).(Palaearctic, Oriental) . . . . . . . . . Megabombus

8 (6) Gonostylus with the inner distal mar-gin simple, flattened, and blade-like in crosssection (Fig. 13r between the lines); antennavery long, reaching distinctly beyond thewing base; hind basitarsus with the posteriorfringe shorter than the greatest breadth of thebasitarsus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

- Gonostylus with the inner distal marginthickened in cross section, with a submarginallongitudinal groove (Fig. 13s between thelines); antenna long, reaching only as faras the posterior margin of the tegula at thewing base; hind basitarsus with the posterior

fringe longer than the greatest breadth of thebasitarsus. (Holarctic) . . . . . . . . Alpinobombus

9 (8) Penis valve head turned outwardsand flattened like an axe head (Fig. 16d cir-cled); gonostylus longer than broad (Fig. 13tcircled); volsella narrow, the inner hooknear the distal end (Fig. 13v circled); hindbasitarsus with an anterior face flattenedproximally, the proximal outer processat the articulation with the tibia stronglyproduced, as long as proximal breadth.(Palaearctic) . . . . . . . . . . . . . . . . . . Kallobombus

- Penis valve head straight, narrowed, andpointed like a spear head (Fig. 16c circled);gonostylus shorter than broad (Fig. 13ucircled); volsella broad, the inner hook nearthe mid point of its length (Fig. 13w circled);hind basitarsus with the anterior marginrounded in section proximally, the proximalouter process at the articulation with thetibia weakly produced, shorter than proximalbreadth. (Oriental) . . . . . . . . . Orientalibombus

10 (5) Gonostylus usually a simple tri-angle, always without an inner proximalprocess (Fig. 13x circled), or if reduced toa single long stout pointed spine (Fig. 13ycircled) then the penis valve head has anouter flange broader than the adjacent penisvalve head and projecting ventrally andlaterally (the rare B. pressus, from the centralHimalaya); gonostylus with the inner distalmargin at least slightly thickened in crosssection with a submarginal longitudinalgroove (similar to Fig. 13s between the lines).(Holarctic, Oriental, northern edge of theNeotropics) . . . . . . . . . . . . . . . . . . . Pyrobombus

- Gonostylus very variable in shape, butusually with a distinct inner proximal process(e.g. Fig. 13l circled), or if this is stronglyreduced or absent (Fig. 13z, aa circled) thenthe distal lobe of the gonostylus is greatlyexpanded distally and projecting inwardlybeyond the volsella (Fig. 13ad, ae arrows)(B. (Cu.) macgregori, from Central America,and B. (Cu.) handlirschi, from the Andes);gonostylus with the inner distal marginsimple, flattened and blade-like in cross


13ab

13af

14a 14b 14c

13ac 13ad 13ae

Figures 13(ab–af)–14(a–c). 13: Male left gonostylus from the dorsal aspect for (ad) B. (Cu.) macgregori;(ae) B. (Cu.) handlirschi; (ab) B. (Ml.) festivus; (ac) B. (Ml.) eximius; (af) B. (Cu.) rufocinctus. 14: Malespatha and penis valves from the dorsal aspect for (a, c) B. (Bo.) patagiatus; (b) B. (Md.) convexus. For allfigures, anterior is towards the bottom of the page and posterior is towards the top. For explanations of thearrows and circles, see the text.

section without a submarginal longitudinalgroove . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

11 (10) Penis valve shaft with a ventralangle about half way along its length anddistinct either as a pronounced sharp angle(Fig. 15d arrow) or produced as a largertransverse process (Fig. 15e circled) . . . . . . 12

- Penis valve shaft with a ventral angleabout half way along its length either re-duced and very broadly rounded (not sharply

marked) or absent (Fig. 15c arrow), althoughthere may be an additional ventral roundedangle at the proximal end of the penis valvehead (most easily confused in e.g. B. (Cu.)rubicundus and B. (Cu.) funebris, from theAndes) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

12 (11) Penis valve head turned inwardsdistally as an incurved bowl-shaped spoon(Fig. 16b circled); penis valve shaft withthe ventral angle about half way alongits length produced ventrally and laterally


15a 15b 15c 15d 15e

16a 16b 16c 16d 16e 16f

17 18a 18b

19a 19b

Figures 15–19. 15: Male left penis valve from the outer lateral aspect for (a) B. (Mg.) trifasciatus; (b) B.(Bo.) lucorum s.l.; (c) B. (Sb.) asiaticus; (d) B. (Ag.) kashmirensis; (e) B. (St.) melanurus. 16: Male left penisvalve from the dorsal aspect for (a) B. (Pr.) hypnorum; (b) B. (St.) melanurus; (c) B. (Or.) haemorrhoidalis;(d) B. (Kl.) soroeensis; (e) B. (Ag.) kashmirensis; (f) B. (Ml.) keriensis. 17: Male left mandible from theouter lateral aspect for B. (Ag.) kashmirensis. 18: Male left volsella from the ventral aspect for (a) B. (Cu.)robustus; (b) B. (Ml.) keriensis. 19: Male left penis valve from the dorsal aspect for (a, b) B. (Cu.) rubicun-dus. For all figures except Figure 17, anterior is towards the bottom of the page and posterior is towards thetop. For explanations of the arrows and circles, see the text.


as a broad transverse paddle-like process(Fig. 15e circled); mandible distally pointedand with one anterior tooth. (Holarctic,Oriental) . . . . . . . . . . . . . . Subterraneobombus

- Penis valve head turned inwards distallyas a dorso-ventrally flattened sickle (Fig. 16ecircled); penis valve shaft with the ventralangle about half way along its length producedventrally as a pronounced angle (Fig. 15darrow); mandible distally pointed and withtwo anterior teeth (Fig. 17 spots). (Palaearctic,Oriental) . . . . . . . . . . . . . . . . . .Alpigenobombus

13 (11) Mid basitarsus on its outer surfacewith many medium and long hairs; gonostyluswith the distal lobe longer or shorter thanbroad; oculo-malar distance longer or shorterthan the breadth of the mandible proximallybetween the outer ends of its articulations(condyles); antenna either medium or long,reaching to or beyond the tegula at the wingbase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

- Mid basitarsus on its outer surfacewith sparse short hairs and very few or nomoderate and long hairs; gonostylus withthe distal lobe always longer than broad;oculo-malar distance always longer than thebreadth of the mandible proximally betweenthe outer ends of its articulations (condyles);antenna usually very long, reaching distinctlybeyond the wing base, or if shorter andreaching only to the posterior margin of thetegula then the recurved hook of the penisvalve head is strongly club-shaped (the rareB. oberti, from Central Asia). (Palaearctic,Oriental) . . . . . . . . . . . . . . . . . . . Sibiricobombus

14 (13) Oculo-malar distance at least aslong as the breadth of the mandible proximallybetween the outer ends of its articulations(condyles); gonocoxa with the inner proximalprocess about as long as broad; either thepenis valve head narrowed as a short slenderbarbed arrow head without a dog-leg (Fig. 16fcircled) (simillimus-lapidarius-group, fromthe Palaearctic and Oriental regions), orthe gonostylus with the shelf of the inner

proximal process membranous (Fig. 13ab cir-cled) (B. festivus, from the Oriental region), orthe gonostylus reduced to a narrow S-shapedband (Fig. 13ac circled) (rufipes-group, fromthe southern Oriental region); volsella, if itis thickened ventrally, then this forms onlya narrow more coarsely-sculptured band ex-tending for most of the length of the volsella(Fig. 18b arrow); antenna of medium length,not reaching beyond the posterior marginof the tegula at the wing base. (Palaearctic,Oriental) . . . . . . . . . . . . . . . . . . . Melanobombus

- Oculo-malar distance shorter than thebreadth of the mandible proximally betweenthe outer ends of its articulations (condyles),or if equal in length then the gonocoxa withthe inner proximal processes finger-like andmore than twice as long as broad (B. coc-cineus, from the Andes); penis valve headeither not narrowed, or if narrowed thenforming an elongated spear head with a smalldog-leg proximally (Fig. 19b circled) (B. ru-bicundus, from the Andes); gonostylus eitherwith a strongly sclerotised inner proximalprocess, or together with the inner distallobe reduced to two small teeth (Fig. 13afcircled) (B. rufocinctus, B. cullumanus, fromthe Holarctic region), or if absent then thedistal lobe is strongly produced distally andinwardly beyond the volsella (Fig. 13ad,ae arrows) (B. handlirschi and B. macgre-gori, from the Andes and Central America);volsella expanded ventrally into a shortpear-shaped coarsely-sculptured thickenedpad in its distal half (Fig. 18a arrow), or ifit is thickened ventrally only as a narrowmore coarsely-sculptured band extending formost of the length of the volsella (similar toFig. 18b arrow) then either the gonostylushas the inner processes reduced to two smallteeth (Fig. 13af circled) (B. rufocinctus,B. cullumanus), or the gonostylus is stronglyproduced distally and inwardly beyond thevolsella (Fig. 13ad arrows) (B. handlirschi,from the Andes); antenna either of mediumlength or longer, reaching to or beyond thetegula at the wing base. (Holarctic, Neotrop-ics) . . . . . . . . . . . . . . . . . . . . Cullumanobombus

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A simplified subgeneric classification of the bumblebees