Abstract
A system of subgenera has been widely used for nearly a century to communicate ideas of relationships 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 process of 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. Using a new strongly-supported estimate of phylogeny for almost all bumblebee species, we apply these criteria to reduce the system to 15 subgenera, and we assess the consequences. Ten new subgeneric synonyms are recognised. Keys to identify adult bumblebees to the simplified subgenera are provided for both sexes.
Zusammenfassung
Hummeln sind farblich sehr variabel, morphologisch ansonsten aber relativ einheitlich. Um die Variation sinnvoll zu ordnen, besteht eine lange Tradition die Arten in Untergattungen zusammenzufassen und sich hierbei zunächst auf die Färbung, dann auf die Morphologie und neuerdings auch auf DNA Sequenzen zu stützen. Allerdings wurde bei 38 Unterarten in den derzeitigen Listungen die Notwendigkeit einer Vereinfachung des Systems gesehen. Wir besprechen die weiterhin bestehende Nützlichkeit des Systems von Untergattungen und erörtern vier mögliche als Leitlinie für Änderungen nutzbare Kriterien. Wir schlagen vor, dass Untergattungen (1) monophyletisch, (2) weniger, (3) aus der Morphologie erkennbar werden sollten und (4) zur Namensgebung wichtiger verhaltensmäßiger oder ökologischer Gruppen dienlich sein sollten. Unter Nutzung einer fast alle Hummeln einschließenden gut fundierten Abschätzung der Phylogenie besprechen wir Konflikte in der Nutzung dieser Kriterien und schlagen ein vereinfachtes System aus 15 Untergattungen vor, in der 10 neue Untergattungssynonyme anerkannt werden. Wir fanden es leicht, monophyletische Subgenera zu erkennen und ihre Anzahl zu reduzieren. Dagegen wurde es mit zunehmender Artenzahl immer schwieriger, Untergattungen zu definieren, die sowohl morphologisch leicht zu unterscheiden waren als auch einige der oft als besonders wichtig angesehenen verhaltensmässigen und ökologischen Eigenschaften teilen. Dies war deshalb der Fall, da entsprechend unserer vorläufigen Analyse einzelne Ausprägungen dieser Eigenschaften nicht ausschließlich von allen Arten einer morphologischen Gruppe geteilt werden.
Similar content being viewed by others
References
Cameron S.A., Whitfield J.B. (1996) Use of walking trails by bees, Nature Lond. 379, 125.
Cameron S.A., Williams P.H. (2003) Phytogeny of bumble bees in the New World subgenus Fervidobombus (Hymenoptera: Apidae): congruence of molecular and morphological data, Mol. Phylogenet. Evol. 28, 552–563.
Cameron S.A., Hines H.M., Williams P.H. (2007) A comprehensive phylogeny of the bumble bees (Bombus), Biol. J. Linn. Soc. 91, 161–188.
Dalla Torre K.W.v. (1880) Unsere Hummel-(Bombus) Arten, Naturhistoriker 2, 40–41.
Dalla Torre K.W.v. (1882) Bemerkungen zur Gattung Bombus Latr., II, Ber. Naturw.-med. Ver. Innsbruck 12, 14–31.
Frison T.H. (1927) A contribution to our knowledge of the relationships of the Bremidae of America north of Mexico (Hymenoptera), Trans. Am. Entomol. Soc. 53, 51–78.
Haas A. (1976) Paarungsverhalten und Nestbau der alpinen Hummelart Bombus mendax (Hymenoptera: Apidae), Entomol. Ger. 3, 248–259.
Hagen E.V., Aichhorn A. (2003) Hummeln: Bestimmen, Ansiedeln, Vermehren, Schützen, Fauna-Verlag, Nottuln.
Harder L.D. (1983) Flower handling efficiency of bumble bees: morphological aspects of probing time, Oecologia 57, 274–280.
Hines H.M., Cameron S.A., Williams P.H. (2006) Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera: Apidae: Bombus) with insights into gene utility for lower-level analysis, Invertebr. Syst. 20, 289–303.
Hines H.M. (in press) Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus), Syst. Biol.
Hobbs G.A. (1964) Phylogeny of bumble bees based on brood-rearing behaviour, Can. Entomol. 96, 115–116.
Hobbs G.A. (1965) Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. II. Subgenus Bombias Robt., Can. Entomol. 97, 120–128.
ICZN (1999) International code of zoological nomenclature, International Commission on Zoological Nomenclature, London.
Ito M. (1985) Supraspecific classification of bumblebees based on the characters of male genitalia, Contr. Inst. Low Temp. Sci. Hokkaido Univ. 20, 1–143.
Kawakita A., Sota T., Ascher J., Ito M., Tanaka H., Kato M. (2003) Evolution and phylogenetic utility of alignment gaps within intron sequences of three nuclear genes in bumble bees (Bombus), Mol. Biol. Evol. 20, 87–92.
Kawakita A., Sota T., Ito M., Ascher J.S., Tanaka H., Kato M., Roubik D.W. (2004) Phylogeny, historical biogeography, and character evolution in bumble bees (Bombus: Apidae) based on simultaneous analysis of three nuclear gene sequences, Mol. Phylogenet. Evol. 31, 799–804.
Kearns C.A., Thomson J.D. (2001) The natural history of bumblebees, a sourcebook for investigations, University Press of Colorado, Boulder.
Kitching I.J., Forey P., Humphries C.J., Williams D. (1998) Cladistics: the theory and practice of parsimony analysis, Oxford University Press, Oxford.
Krüger E. (1917) Zur Systematik der mitteleuropäischen Hummeln (Hym.), Entomol. Mitt. 6, 55–66.
Krüger E. (1920) Beiträge zur Systematik und Morphologie der mitteleuropäischen Hummeln, Zool. Jb., Abt. Syst. 42, 289–464.
Kruseman G. (1952) Subgeneric division of the genus Bombus Latr, Trans. 9th Int. Congr. Entomol., Amsterdam, pp. 101–103
Latreille P.A. (1802) Histoire naturelle des fourmis, et recueil de mémoires et d’observations sur les abeilles, les araignées, les faucheurs, et autres insectes, Paris, Impr. F. Dufart.
Løken A. (1973) Studies on Scandinavian bumble bees (Hymenoptera, Apidae), Norsk Entomol. Tiddskr. 20, 1–218.
Medler J.T. (1962) Morphometric studies on bumble bees, Ann. Entomol. Soc. Am. 55, 212–218.
Menke A.S., Carpenter J. (1984) Nuclearbombus, new subgenus (or how to eliminate bumblebee subgenera and learn to love Bombus), Sphecos 9, 28.
Michener C.D. (1990) Classification of the Apidae (Hymenoptera), Kans. Univ. Sci. Bull. 54, 75–164.
Michener C.D. (1997) Genus-group names of bees and supplemental family group names, Sci. Pap. Nat. Hist. Mus. Univ. Kans. 1, 1–81.
Michener C.D. (2000) The bees of the world, John Hopkins University Press, Baltimore.
Michener C.D. (2007) The bees of the world, John Hopkins University Press, Baltimore.
Milliron H.E. (1961) Revised classification of the bumblebees — a synopsis (Hymenoptera: Apidae), J. Kans. Entomol. Soc. 34, 49–61.
Milliron H.E. (1971) A monograph of the western hemisphere bumblebees (Hymenoptera: Apidae; Bombinae). I. The genera Bombus and Megabombus subgenus Bombias, Mem. Entomol. Soc. Can. 82, 1–80.
Milliron H.E. (1973a) A monograph of the western hemisphere bumblebees (Hymenoptera: Apidae; Bombinae). II. The genus Megabombus subgenus Megabombus, Mem. Entomol. Soc. Can. 89, 81–237.
Milliron H.E. (1973b) A monograph of the western hemisphere bumblebees (Hymenoptera: Apidae; Bombinae). III. The genus Pyrobombus subgenus Cullumanobombus, Mem. Entomol. Soc. Can. 91, 238–333.
Pedersen B.V. (2002) European bumblebees (Hymenoptera: Bombini) — phylogenetic relationships inferred from DNA sequences, Insect Syst. Evol. 33, 361–386.
Pittioni B. (1939) Die Hummeln und Schmarotzerhummeln der Balkan-Halbinsel. II. Spezieller Teil, Mitt. k. Nat. Wiss. Inst. Sofia 12, 49–115.
Pittioni B. (1949) Beiträge zur Kenntnis der Bienenfauna SO-Chinas. Die Hummeln und Schmarotzerhummeln der Ausbeute J. Klapperich (1937/38). (Hym., Apoidea, Bombini), Eos, Madr. 25, 241–284.
Plath O.E. (1927) The natural grouping of the Bremidae (Bombidae) with special reference to biological characters, Biol. Bull. 52, 394–410.
Plath O.E. (1934) Bumblebees and their ways, MacMillan, New York.
Plowright R.C. (1977) Nest architecture and the biosystematics of bumble bees, Proc. 8th Int. Congr. IUSSI, 183–185.
Popov V.B. (1931) Zur Kenntnis der paläarktischen Schmarotzerhummeln (Psithyrus Lep.), Eos, Madr. 7, 131–209.
Prys-Jones O.E., Corbet S.A. (1987) Bumblebees, Cambridge University Press, Cambridge.
Radoszkowski O. (1884) Révision des armures copulatrices des mâles du genre Bombus, Byull. Mosk. Obshch. Ispyt. Prir. 59, 51–92.
Rasmont P. (1983) Catalogue commenté des bourdons de la région ouest-paléarctique (Hymenoptera, Apoidea, Apidae), Notes Fauniques de Gembloux 7, 1–71.
Rasmont P. (1988) Monographie écologique et zoogéographique des bourdons de France et de Belgique (Hymenoptera, Apidae, Bombinae), 309 p.+lxi, Faculté des Sciences agronomiques de l’État, Gembloux.
Rasmont P., Terzo M., Aytekin A.M., Hines H.M., Urbanova K., Cahlikova L., Valterova I. (2005) Cephalic secretions of the bumblebee subgenus Sibiricobombus Vogt suggest Bombus niveatus Kriechbaumer and Bombus vorticosus Gerstaecker are conspecific (Hymenoptera, Apidae, Bombus), Apidologie 36, 571–584.
Reinig W.F. (1981) Synopsis der in Europa nachgewiesenen Hummel- und Schmarotzerhummelarten (Hymenoptera, Bombidae), Spixiana 4, 159–164.
Richards K.W. (1973) Biology of Bombus polaris Curtis and B. hyperboreus Schönherr at Lake Hazen, Northwest Territories (Hymenoptera: Bombini), Quaest. Entomol. 9, 115–157.
Richards K.W. (1975) Population ecology of bumblebees in southern Alberta, University of Kansas, Lawrence, p. 117.
Richards O.W. (1929) A revision of the humble-bees allied to Bombus orientalis, Smith, with the description of a new subgenus, Ann. Mag. Nat. Hist. 3, 378–386.
Richards O.W. (1968) The subgeneric divisions of the genus Bombus Latreille (Hymenoptera: Apidae), Bull. Br. Mus. Nat. Hist. (Entomol.) 22, 209–276.
Robertson C. (1903) Synopsis of Megachilidae and Bombinae, Trans. Am. Entomol. Soc. 29, 163–178.
Sakagami S.F. (1976) Specific differences in the bionomic characters of bumblebees. A comparative review, J. Fac. Sci. Hokkaido Univ. (Zool.) 20, 390–447.
Sandhouse G.A. (1943) The type species of the genera and subgenera of bees, Proc. U.S. Nat. Mus. 92, 519–619.
Skorikov A.S. (1914) Les formes nouvelles des bourdons (Hymenoptera, Bombidae). VI, Russk. Entomol. Obozr. 14, 119–129.
Skorikov A.S. (1922) Bumblebees of the Petrograd Province, Faunae Petropolitanae catalogus, Petrogradskii Agronomicheskii Institut, Petrograd, 51 p. [in Russian].
Skorikov A.S. (1923) Palaearctic bumblebees. Part I. General biology (including zoogeography), Izv. Sev. Oblast. Sta. Zashch. Rast. Vredit. 4 (1922), 1–160 [in Russian].
Skorikov A.S. (1931) Die Hummelfauna Turkestans und ihre Beziehungen zur zentralasiatischen Fauna (Hymenoptera, Bombidae), in: Lindholm V.A. (Ed.), Abhandlungen der Pamir-Expedition 1928, Academy of Sciences of the USSR, Leningrad, pp. 175–247.
Sladen F.W.L. (1912) The humble-bee, its life history and how to domesticate it, with descriptions of all the British species of Bombus and Psithyrus, MacMillan, London.
Stevens P.F. (2006) Angiosperm phylogeny website. Version 7, May 2006 [online] http://www.mobot.org/MOBOT/research/APweb/ (accessed on 12 November 2007).
Terzo M., Coppens P., Valterova I., Toubeau G., Rasmont P. (2005) Does behaviour replace male scent marking in some bumble bees? Evidence of the absence of sexual marking cephalic secretion in the subgenus Rhodobombus, 21st Annu. Meet. Int. Soc. Chem. Ecol., p. 145
Terzo M., Coppens P., Valterova I., Toubeau G., Rasmont P. (2007a) Reduced cephalic labial glands in the male bumblebees of the subgenus Rhodobombus Dalla Torre (Hymenoptera, Apidae, Bombus Latreille), Ann. Soc. Entomol. Fr. 43, 497–503.
Terzo M., Valterova I., Rasmont P. (2007b) Atypical secretions of the male cephalic labial glands in bumblebees: the case of Bombus (Rhodobombus) mesomelas Gerstaecker (Hymenoptera, Apide), Chem. Biodiv. 4, 1466–1471.
Thorp R.W., Horning D.S., Dunning L.L. (1983) Bumble bees and cuckoo bumble bees of California (Hymenoptera: Apidae), Bull. Calif. Insect Surv. 23, viii+79.
Tkalců B. (1972) Arguments contre l’interprétation traditionnelle de la phylogénie des abeilles (Hymenoptera, Apoidea). Première partie, introduction et exposés fondamentaux, Bull. Soc. Entomol. Mulhouse 1972, 17–28.
Vogt O. (1911) Studien über das Artproblem. 2. Mitteilung. Über das Variieren der Hummeln. 2. Teil. (Schluss), Sitz.ber. Ges. Naturforsch. Freunde Berl. 1911, 31–74.
Walter D.E., Winterton S. (2007) Keys and the crisis in taxonomy: extinction or reinvention? Annu. Rev. Entomol. 52, 193–208.
Williams P.H. (1985) A preliminary cladistic investigation of relationships among the bumble bees (Hymenoptera, Apidae), Syst. Entomol. 10, 239–255.
Williams P.H. (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini), Bull. Br. Mus. Nat. Hist. (Entomol.) 60, 1–204.
Williams P.H. (1995) Phylogenetic relationships among bumble bees (Bombus Latr.): a reappraisal of morphological evidence, Syst. Entomol. 19, 327–344.
Williams P.H. (1998) An annotated checklist of bumble bees with an analysis of patterns of description (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., Day L., Ascher J., Buchmann S. (2006) Importation of non-native bumble bees into North America: potential consequences of using Bombus terrestris and other non-native bumble bees for greenhouse crop pollination in Canada, Mexico, and the United States, p. 33, A White Paper of the North American Pollinator Protection Campaign (NAPCC).
Author information
Authors and Affiliations
Corresponding author
Additional information
Manuscript editor: E.A.B. Almeida
Rights and permissions
About this article
Cite this article
Williams, P.H., Cameron, S.A., Hines, H.M. et al. A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie 39, 46–74 (2008). https://doi.org/10.1051/apido:2007052
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1051/apido:2007052