A simplified protocol for bumble bee species identification by cephalic secretion analysis

Insectes Sociaux

Volumn 58, Issue 2, 2011, Pages 227-236

  de Meulemeester, T ^a   Gerbaux, P ^a   Boulvin, M ^a   Coppee A ^a   Rasmont, P ^a  

^a UNIVERSITY OF MONS   (Belgium)

Author keywords

Bombus ignitus ignitus; Bombus terrestris dalmatinus; Bumble bees; Labial gland secretion; Sex pheromones

Indexed keywords

BEE; CLUSTER ANALYSIS; GAS CHROMATOGRAPHY; IDENTIFICATION METHOD; MASS SPECTROMETRY; SECRETION; SEX PHEROMONE;

BOMBUS (GENUS); BOMBUS IGNITUS; BOMBUS TERRESTRIS;

EID: 79952705357     PISSN: 00201812     EISSN: 14209098     Source Type: Journal    
DOI: 10.1007/s00040-011-0146-1     Document Type: Article

References (46)

1. Ågren L., Cederberg B. and Svensson B. G. 1979. Changes with age in ultrastructure and pheromone content of male labial glands in some bumble bee species (Hymenoptera, Apidae). Zoon7: 1-14.
2. Aytekin A. M., Terzo M., Rasmont P. and Çaǧatay N. 2007. Landmark based geometric morphometric analysis of wing shape in Sibiricobombus Vogt (Hymenoptera: Apidae: Bombus Latreille). Ann. Soc. entomol. Fr. (n. s.)43: 95-102.
3. Bagnères A-G. and Wicker-Thomas C. 2010. Chemical taxonomy with hydrocarbons. In: Insect Hydrocarbons - Biology, Biochemistry, and Chemical Ecology (Blomquist G. J. and Bagnères A-G., Eds), Cambridge University Press, New-York. pp 121-162.
4. Bergström G. and Svensson B. G. 1973. 2, 3-Dihydro-6, trans-farnesol: main component in the cephalic marker secretion of Bombus jonellus K. (Hym., Apidae) males. Zoon Suppl. 1: 61-65.
5. Bergström G., Kullenberg B. and Ställberg-Stenhagen S. 1973. Studies on natural odoriferous compounds. VII. Recognition of two forms of Bombus lucorum L. (Hymenoptera, Apidae) by analysis of the volatile marking secretion from individual males. Chem. scripta4: 174-182.
6. Bertsch A. 1997. Abgrenzung der Hummel-Arten Bombus cryptarum und B lucorum mittels männlicher Labialdrüsen-Sekrete und morphologischer Merkmale (Hymenoptera, Apidae). Entomol. Gen. 22: 129-145.
7. Bertsch A., Schweer H., Titze A. and Tanaka H. 2005. Male labial gland secretions and mitochondrial DNA markers support, species status of Bombus cryptarum and B. magnus (Hymenoptera, Apidae). Insect. Soc. 52: 45-54.
8. Blum M. S., Fales H. M., Morse R. A. and Underwood B. A. 2000. Chemical characters of two related species of giant honeybees (Apis dorsata and A. laboriosa): Possible ecological significance. J. Chem. Ecol. 26: 801-807.
9. Bruschini C., Cervo R., Dani F. R. and Turillazzi S. 2007. Can venom volatiles be a taxonomic tool for Polistes wasps (Hymenoptera, Vespidae)? J. Zool. Syst. Evol. Res. 45: 202-205.
10. Calam D. H. 1969. Species and sex-specific compounds from the heads of male bumblebees (Bombus spp.). Nature221: 856-857.
11. Cameron S. A., Hines H. M. and Williams P. H. 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linnean Soc. 91: 161-188.
12. Claudet J., Pelletier D., Jouvenel J. Y., Bachet F. and Galzin R. 2006. Assessing the effects of marine protected area (MPA) on a reef fish assemblage in a northwestern Mediterranean marine reserve: Identifying community-based indicators. Biol. Conserv. 130: 349-369.
13. Coppée A., Terzo M., Valterová I. and Rasmont P. 2008. Intraspecific variation of the cephalic labial gland secretions in Bombus terrestris (L.) (Hymenoptera: Apidae). Chem. Biodivers. 5: 2654-2661.
14. Dahbi A., Hefetz A. and Lenoir A. 2008. Chemotaxonomy of some Cataglyphis ants from Morocco and Burkina Faso. Biochem. Syst. Ecol. 36: 564-572.
15. Dufrêne M. and Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67: 346-366.
16. Ellis J. S., Knight M. E. and Goulson D. 2005. Delineating species for conservation using mitochondrial sequence data: the taxonomic status of two problematic Bombus species (Hymenoptera: Apidae). J. Insect Conserv. 9: 75-83.
17. Ellis J. S., Knight M. E., Carvell C. and Goulson D. 2006. Cryptic species identification: a simple diagnostic tool for discriminating between two problematic bumblebee species. Mol. Ecol. Notes6: 540-542.
18. Estoup A., Solignac M., Cornuet J. M., Goudet J. and Scholl A. 1996. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 5: 19-31.
19. Haverty M. I., Page M., Nelson L. J. and Blomquist G. J. 1988. Cuticular hydrocarbons of dampwood termites, Zootermopsis: Intra- and intercolony variation and potential as taxonomic characters. J. Chem. Ecol. 14: 1035-1058.
20. Haverty M. I., Woodrow R. J., Nelson L. J. and Grace J. K. 2005. Identification of termite species by the hydrocarbons in their feces. J. Chem. Ecol. 31: 2119-2151.
21. Ito M. 1987. Geographic variation of an eastern Asian bumble bee Bombus diversus in some morphometric characters (Hymenoptera, Apidae). Kontyu55: 188-201.
22. Kanbe Y., Okada I., Yoneda M., Goka K. and Tsuchida K. 2008. Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften95: 1003-1008.
23. Kindl J., Hovorka O., Urbanová K. and Valterová I. 1999. Scent marking in male premating behavior of Bombus confusus. J. Chem. Ecol. 25: 1489-1500.
24. Kondo N. I., Yamanaka D., Kanbe Y., Kunitake Y. K., Yoneda M., Tsuchida K. and Goka K. 2009. Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris. Naturwissenschaften96: 467-475.
25. Kullenberg B., Bergström G., Bringer B., Carlberg B. and Cederberg B. 1973. Observations on scent marking by Bombus Latr. and Psithyrus Lep. Males (Hym., Apidae) and localization of site of production of the secretion. Zoon Suppl. 1: 23-30.
26. Lucas C., Fresneau D., Kolmer K., Heinze J., Delabie J. H. C. and Pho D. B. 2002. A multidisciplinary approach to discriminating different taxa in the species complex Pachycondyla villosa (Formicidae). Biol. J. Linn. Soc. 75: 249-259.
27. MacQueen J. B. 1967. Some Methods for classification and analysis of multivariate observations. In: Proc. 5th Berkeley Symp. Math, Statistics, and Probability, University of California Press. pp 281-297.
28. Martin S. J., Helanterä H. and Drijfhout F. P. 2008. Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol. J. Linn. Soc. 95: 131-140.
29. Murray T. E., Fitzpatrick U., Brown M. J. F. and Paxton R. J. 2008. Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Conserv. Genet. 9: 653-666.
30. Paterson H. E. H. 1985. The recognition concept of species. In: Species and Speciation (Vrba E. S., Ed), Transvaal Museum Monograph No. 4, Transvaal Museum, Pretoria. pp 21-29.
31. Paterson H. E. H. 1993. Evolution and the Recognition Concept of Species. The Johns Hopkins University Press, Baltimore. 234 pp.
32. R Development Core Team, 2009. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www. R-project. org.
33. Rasmont P., Terzo M., Aytekin A. M., Hines H., Urbanová K., Cahliková L. and Valterová I. 2005. Cephalic secretions of the bumblebee subgenus Sibiricobombus Vogt suggest Bombus niveatus Kriechbaumer and Bombus vorticosus Gerstaecker are conspecific (Hymenoptera, Apidae, Bombus). Apidologie36: 571-584.
34. Reynolds T. 2007. The evolution of chemosystematics. Phytochemistry68: 2887-2895.
35. Schlick-Steiner B. C., Steiner F. M., Seifert B., Stauffer C., Christian E. and Crozier R. H. 2010. Integrative taxonomy: a multisource approach to exploring biodiversity. Annu. Rev. Entomol. 55: 421-438.
36. Šobotnik J., Kalinová B., Cahliková L., Weyda F., Ptáček V. and Valterová I. 2008. Age-dependent changes in structure and function of the male labial gland in Bombus terrestris. J. Insect Physiol. 54: 204-214.
37. Svensson B. G. 1979. Pyrobombus lapponicus auct., in Europe recognized as two species: P. lapponicus (Fabricius, 1793) and P. monticola (Smith, 1849) (Hymenoptera, Apoidea, Bombinae). Insect Syst. Evol. 10: 275-296.
38. Svensson B. G. 1980. Species-Isolating Mechanisms in Male Bumble Bees (Hymenoptera, Apidae). Acta Universitatis Upsaliensis, Uppsala. 42 pp.
39. Svensson B. G. and Bergström G. 1977. Volatile marking secretions from the labial gland of north European Pyrobombus D. T. males (Hymenoptera, Apidae). Insect. Soc. 24: 213-224.
40. Terzo M., Valterová I., Urbanová K. and Rasmont P. 2003. De la nécessité de redécrire les phéromones sexuelles des mâles de bourdons (Hymenoptera, Apidae, Bombini) publiées avant 1996 pour leur utilisation en analyse phylogénétique. Phytoprotection84: 39-49.
41. Terzo M., Urbanová K., Valterová I. and Rasmont P. 2005. Intra and interspecific variability of the cephalic labial glands' secretions in male bumblebees: the case of Bombus (Thoracobombus) ruderarius and B. (Thoracobombus) sylvarum (Hymenoptera, Apidae). Apidologie36: 85-96.
42. Terzo M., Valterová I. and Rasmont P. 2007a. Atypical secretions of the male cephalic labial glands in bumblebees: The case of Bombus (Rhodobombus) mesomelas Gerstaecker (Hymenoptera, Apidae). Chem. Biodivers. 4: 1466-1471.
43. Terzo M., Coppens P., Valterová I., Toubeau G. and Rasmont P. 2007b. Reduced cephalic labial glands in the male bumblebees of the subgenus Rhodobombus Dalla Torre (Hymenoptera: Apidae: Bombus Latreille). Ann. Soc. entomol. Fr. (n. s.)43: 497-503.
44. 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/entomology/bombus].
45. Williams P. H. and Hernandez L. 2000. Distinguishing females of the bumble bees Bombus ruderatus (F.) from Bombus hortorum (L.) in Britain: a preliminary application of quantitative techniques. In: Report to the UK Biodiversity Action Plan (Bumblebee working group). 25 pp.
46. Žáček P., Kalinová B., Šobotnik J., Hovorka O., Ptáček V., Coppée A., Verheggen F. and Valterova I. 2009. Comparison of age-dependent quantitative changes in the male labial gland secretion of Bombus terrestris and Bombus lucorum. J. Chem. Ecol. 35: 698-705.