Skip to main content
SpringerLink
Log in

Variability in Sexual Pheromones Questions their Role in Bumblebee Pre-Mating Recognition System

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Sex-specific chemical secretions have been widely used as diagnostic characters in chemotaxonomy. The taxonomically confused group of bumblebees has reaped the benefit of this approach through the analyses of cephalic labial gland secretions (CLGS). Most of currently available CLGS descriptions concern species from the West-Palearctic region but few from the New World. Here, the CLGS of four East-Palearctic species Bombus deuteronymus, B. filchnerae, B. humilis, and B. exil (subgenus Thoracobombus) are analysed. Our results show high levels of variability in the major compounds in B. exil. In contrast, we describe a low differentiation in CLGS compounds between B. filchnerae and its phylogenetically closely related taxon B. muscorum. Moreover, the chemical profiles of B. filchnerae and B. muscorum are characterized by low concentrations of the C16 component, which is found in higher concentrations in the other Thoracobombus species. This raises the possibility that courtship behavior as well as environmental constraints could affect the role of the bumblebee males’ CLGS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • An J, Huang J, Shao Y, Zhang S, Wang B, Liu X, Wu J, Williams PH (2014) The bumblebees of North China (Apidae, Bombus Latreille). Zootaxa 3880:001–089

    Article  Google Scholar 

  • Ayasse M, Jarau S (2014) Chemical ecology of bumble bees. Annu Rev Entomol 59:299–319

    Article  CAS  PubMed  Google Scholar 

  • Bagnères AG, Uva P, Clément JL (2003) Description d’une nouvelle espèce de Termite: Reticulitermes urbis n.sp. (Isopt., Rhinotermitidae). Bull Soc Entomol Fr 108:433–435

    Google Scholar 

  • Bergström G, Svensson BG, Appelgren M, Groth I (1981) Complexity of bumble bee marking pheromones: biochemical, ecological and systematical interpretations. SystAss special vo:175–183

  • Bertsch A, Schweer H (2011) Labial gland marking secretions of male Bombus lucorum bumblebees from Europe and China reveal two separate species: B. lucorum (Linnaeus 1761) and Bombus minshanicola (Bischoff 1936). Biochem Syst Ecol 39:587–593

    Article  CAS  Google Scholar 

  • Bertsch A, Schweer H, Titze A (2004) Analysis of the labial gland secretions of the male bumblebee Bombus griseocollis (hymenoptera: Apidae). Z Naturforsch - section C J Biosci 59:701–707

    CAS  Google Scholar 

  • Bertsch A, Schweer H, Titze A (2008) Chemistry of the cephalic labial gland secretions of male Bombus morrisoni and B. rufocinctus, two north American bumblebee males with perching behavior. J Chem Ecol 34:1268–1274

    Article  CAS  PubMed  Google Scholar 

  • Brasero N, Martinet B, Urbanová K, Valterová I, Torres A, Hoffmann W, Rasmont P, Lecocq T (2015) First chemical analysis and characterization of the male species-specific cephalic labial-gland secretions of south American bumblebees. Chem Biodivers 12:1535–1546

    Article  CAS  PubMed  Google Scholar 

  • Brasero N, Martinet B, Lecocq T, Lhomme P, Biella P, Valterova I, Urbanova K, Cornalba M, Hines H, Rasmont P (2017) The cephalic labial gland secretions of two socially parasitic bumblebees Bombus hyperboreus (Alpinobombus) and Bombus inexspectatus (Thoracobombus) question their inquiline strategy. Insect Sci 00:1–12

    Google Scholar 

  • Brill MF, Rosenbaum T, Reus I, Kleineidam CJ, Nawrot MP, Rössler W (2013) Parallel processing via a dual olfactory pathway in the honeybee. J Neurosci 33:2443–2456

    Article  CAS  PubMed  Google Scholar 

  • Calam DH (1969) Species and sex-specific compounds from the heads of male bumblebees (Bombus spp.) Nature 221:856–857

    Article  CAS  PubMed  Google Scholar 

  • Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linnean Soc 91:161–188

    Article  Google Scholar 

  • Carcaud J, Hill T, Guirfa M, Sandoz J-C (2012) Differential coding by two olfactory subsystems in the honeybee brain. J Neurophysiol 108:1106–1121

    Article  PubMed  Google Scholar 

  • Carcaud J, Giurfa M, Sandoz J-C (2015) Differential combinatorial coding of pheromones in two olfactory subsystems of the honey bee brain. J Neurosci 35:4157–4167

    Article  CAS  PubMed  Google Scholar 

  • Cicolella A (2008) Les composés organiques volatils (COV): définition, classification et propriétés. Rev Mal Respir 25:155–163

    Article  CAS  PubMed  Google Scholar 

  • Claudet J, Pelletier D, Jouvenel JY, Bachet F, 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

    Article  Google Scholar 

  • Cvacka J, Kofronová E, Vasícková S, Stránský K, Jiros P, Hovorka O, Kindl J, Valterová I (2008) Unusual fatty acids in the fat body of the early nesting bumblebee, Bombus pratorum. Lipids 43:441–450

    Article  CAS  PubMed  Google Scholar 

  • Dalla Torre KW (1880) Unsere Hummel-(Bombus) Arten. Die Naturhistoriker 30:40–41

    Google Scholar 

  • Darvill B, Lye GC, Goulson D (2007) Aggregations of male Bombus muscorum (hymenoptera: Apidae) at mature nest. Incestuous brothers or amorous suitors? Apidologie 38:518–524

    Article  Google Scholar 

  • De Meulemeester T, Gerbaux P, Boulvin M, Coppée A, Rasmont P (2011) A simplified protocol for bumble bee species identification by cephalic secretion analysis. Insect Soc 58:227–236

    Article  Google Scholar 

  • Dellicour S, Lecocq T (2013a) GCALIGNER 1.0 and GCKOVATS 1.0 - manual of a software suite to compute a multiple sample comparison data matrix from eco-chemical datasets obtained by gas chromatography. University of Mons, Mons

  • Dellicour S, Lecocq T (2013b) GCALIGNER 1.0: a aligment program to compute a multiple sample comparison data matrix from large eco-chemical datasets obtained by gas chromatography. J Sep Sci 36:3206–3209

    CAS  PubMed  Google Scholar 

  • Djegham Y, Verhaeghe JC, Rasmont P (1994) Copulation of Bombus terrestris L. (hymenoptera: Apidae) in captivity. J Apic Res 33:15–20

    Article  Google Scholar 

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Dumas P, Tetreau G, Petit D (2010) Why certain male grasshoppers have clubbed antennae? C R Biol 335(5):429–437

    Article  Google Scholar 

  • Felicioli A (1998) Ethological and morphological analysis of mating behaviour in Osmia cornuta Latr. (hymenoptera, Megachilidae). Ins. Soc. Life 2:137–144

    Google Scholar 

  • Fonta C, Masson C (1984) Comparative study by electrophysiology of olfactory responses in bumblebees (Bombus hypnorum and Bombus terrestris). J Chem Ecol 10:1157–1168

    Article  CAS  PubMed  Google Scholar 

  • Galizia CG, Menzel R (2001) The role of glomeruli in the neural representation of odours: results from optical recording studies. J Insect Physiol 47:115–130

  • Hay ME (2011) Crustaceans as powerful models in aquatic chemical ecology. In: Thiel TB and M (ed) chemical communication in crustaceans. Springer, New York, pp 41–62

    Google Scholar 

  • Krüger E (1951) Über die Bahnflüge der Männchen der Gattungen Bombus und Psithyrus. Z Tierpsychol 8:61–75

    Article  Google Scholar 

  • Lecocq T, Lhomme P, Michez D, Dellicour S, Valterová I, Rasmont P (2011) Molecular and chemical characters to evaluate species status of two cuckoo bumblebees: Bombus barbutellus and Bombus maxillosus (hymenoptera, Apidae, Bombini). Syst Entomol 36:453–469

    Article  Google Scholar 

  • Lecocq T, Vereecken NJ, Michez D, Dellicour S, Lhomme P, Valterová I, Rasplus J-Y, Rasmont P (2013) Patterns of genetic and reproductive traits differentiation in mainland vs. Corsican populations of bumblebees. PLoS One 8:e65642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lecocq T, Coppée A, Mathy T, Lhomme P, Cammaerts-Tricot MC, Urbanová K, Valterová I, Rasmont P (2015a) Subspecific differentiation in male reproductive traits and virgin queen preferences, in Bombus terrestris. Apidologie 26:595–605

    Article  Google Scholar 

  • Lecocq L, Brasero N, Martinet B, Valterova I, Rasmont P (2015b) Highly polytypic taxon complex: interspecific and intraspecific integrative taxonomic assessment of the widespread pollinator Bombus pascuorum Scopoli 1763 (hymenoptera: Apidae). Syst Entomol 40:881–890

    Article  Google Scholar 

  • Lecocq T, Dellicour S, Michez D, Dehon M, Dewulf A, De Meulemeester T, Brasero N, Valterová I, Rasplus JY, Rasmont P (2015c) Methods for species delimitation in bumblebees (hymenoptera, Apidae, Bombus): towards an integrative approach. Zool Scr 44:1–17

    Article  Google Scholar 

  • Lecocq T, Brasero N, De Meulemeester T, Michez D, Dellicour S, Lhomme P, de Jonghe R, Valterová I, Urbanová K, Rasmont P (2015d) An integrative taxonomic approach to assess the status of Corsican bumblebees: implications for conservation. Anim Conserv 18:236–148

    Article  Google Scholar 

  • Lhomme P, Sramkova A, Kreuter K, Lecocq T, Rasmont P, Ayasse M (2013) A method for year-round rearing of cuckoo bumblebees (hymenoptera : Apoidea : Bombus subgenus Psithyrus ). Ann Soc entomol Fr (N.S.) 49:37–41

  • Lhomme P, Ayasse M, Valterová I, Lecocq T, Rasmont P (2015) A scent shield to survive: identification of the repellent compounds secreted by the male offspring of the cuckoo bumblebee Bombus vestalis. Entomol Exp Appl 157:263–270

    Article  CAS  Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Holmiae. 823 pp

  • Lockey KH (1991) Insect hydrocarbon classes: implications for chemotaxonomy. Insect Biochem 21:91–97

    Article  CAS  Google Scholar 

  • Luxová A, Valterová I, Stránský K, Hovorka O, Svatoš A (2003) Biosynthetic studies on marking pheromones of bumblebee males. Chemoecology 13:81–87

    Article  Google Scholar 

  • Martinet B, Lecocq T, Brasero N, Biella P, Urbanová K, Valterová I, Cornalba M, Gjershaug JO, Michez D, Rasmont P (2017) Following the cold: geographic differentiation between interglacial refugia and speciation in arcto-alpine species complex Bombus monticola (Hymenoptera: Apidae). Syst Entomol (in press)

  • Michener CD (1990) Classification of the Apidae (hymenoptera). Univ Kans publ, Mus Nat Hist 54:75–164

    Google Scholar 

  • Oksanen FJ, Blanchet G, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Tertiary Vegan: Community Ecology Package

  • Paterson H (1993) Evolution and the recognition concept of species. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Patricelli GL, Uy JAC, Borgia G (2003) Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds. Proc R Soc Lond B Biol Sci 270:2389–2395

  • Pokorny T, Lunau K, Quezada-Euan JJG (2014) Cuticular hydrocarbons distinguish cryptic sibling species in Euglossa orchid bees. Apidologie 45:276–283

    Article  CAS  Google Scholar 

  • Quicke DJ (1993) Chemotaxonomy and Related Topics. In: Principles and Techniques of Contemporary Taxonomy. Experimental and Clinical Neuroscience. Springer, Dordrecht, pp 146-154

  • R Development Core Team (2017) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org

  • Rasmont P, Terzo M, Aytekin AM, Hines H, Urbanová K, Cahliková L, Valterová 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

    Article  Google Scholar 

  • Romani R, Isidoro N, Riolo P, Bin F (2003) Antennal glands in males bees: structures for sexual communication by pheromones? Apidologie 34:603–610

    Article  Google Scholar 

  • Sachse S, Rappert A, Galizia CG (1999) The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. J Neurosci 11:3970–3982

    CAS  Google Scholar 

  • Sandoz JC (2012) Olfaction in honey bees: from molecules to behavior. In: Galizia G, Eisenhardt D, Giurfa M (eds) Honeybee neurobiology and behavior. A tribute to Randolf Menzel. Springer, Dordrecht, pp 235–252

    Chapter  Google Scholar 

  • Sandoz JC, Deisig N, de Brito Sanchez MG, Giurfa M (2007) Understanding the logics of pheromone processing in the honeybee brain: from labeledlines to across-fiber patterns. Front Behav Neurosci 1:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Skorikov AS (1914) Les formes nouvelles des bourdons (Hymenoptera, Bombidae). V Russkoe éntomologicheskoe Obozrênie 14:119–129

    Google Scholar 

  • Skorikov AS (1923) Palaearctic bumblebees. Part I. General biology (including zoogeography). Izv Severn Obl Stantsii Zashch Rast Vredit 4:1–160

  • Strube-Bloss MF, Brown A, Spaethe J, Schmitt T, Rössler W (2015) Extracting the behaviorally relevant stimulus: unique neural representation of farnesol, a component of the recruitment pheromone of Bombus terrestris. PLoS One 10:e0137413

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki R, Shimodaira H (2011) Pvclust: hierarchical clustering with P-values via multiscale bootstrap resampling. Contributed package. Version 1-1.10. Vienna, R foundation for statistical computing. http://www.R-project.org

  • Svensson BG, Bergström G (1977) Volatile marking secretions from the labial gland of north European Pyrobombus D. T. Males (hymenoptera, Apidae). Insect Soc 24:213–224

    Article  CAS  Google Scholar 

  • Svensson BG, Bergström G (1979) Marking pheromones of Alpinobombus males. J Chem Ecol 5:603–615

    Article  CAS  Google Scholar 

  • Symonds MRE, Moussalli A, Elagar MA (2009) The evolution of sex pheromones in an ecologically diverse genus of flies. Biol J Linn Soc 9:594–603

    Article  Google Scholar 

  • Tasei JN, Moinard C, Moreau L, Himpens B, Guyonnaud S (1998) Relationship between aging, mating and sperm production in captive Bombus terrestris. J Apic Res 37:107–113

    Article  Google Scholar 

  • Terzo M, Valterová I, Urbanová K, 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. Phytoprotection 84:39–49

    Article  CAS  Google Scholar 

  • Terzo M, Urbanová K, Valterová I, 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. Apidologie 36:85–96

    Article  Google Scholar 

  • Terzo M, Valterová I, Rasmont P (2007) Atypical secretions of the male cephalic labial glands in bumblebees: the case of Bombus (Rhodobombus) mesomelas Gerstaecker (hymenoptera, Apidae). Chem Biodivers 4:1466–1471

    Article  CAS  PubMed  Google Scholar 

  • Tkalců B (1974) Ergebnise der 1. Und 2. Mongolisch-tschechoslowakischen entomologisch-botanischen expedition in der Mongolei nr. 29: hymenoptera, Apoidea, Bombinae. – Acta faunistica entomologica Musei Nationalis Pragae 15: 25-58

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, Queensland

    Book  Google Scholar 

  • Vogt O (1908) Bombi (Hummeln). Wissenschaftliche Ergebnisse von Expedition Filchner nach China und Thibet 1903-1905, X. Band - I. Teil, 1. Abschnitt: Zoologische Sammlungen, Berlin.100–101

  • Vogt O (1911) Studien über das Artproblem. 2. Mitteilung. über das Variieren der Hummeln. 2. Teil (Schluss). Schriften der berlinischen Gesellschaft Naturforschender, Freunde, Berlin 1911:31–74

    Google Scholar 

  • Williams PH (1998) An annotated checklist of bumble bees with an analysis of patterns of description (hymenoptera: Apidae, Bombini). Bulletin of The Natural History Museum (Entomology) 67: 79–152. Updated at www.nhm.ac.uk/bombus/ accessed 2017

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Yin X-W, Immacolata I, Marangoni R, Cattonaro F, Flamini G, Sagona S, Zhang L, Pelosi P, Felicioli A (2013) Odorant-binding proteins and olfactory coding in the solitary bee Osmia cornuta. Cell Mol Life Sci 70:3029–3039

    Article  CAS  PubMed  Google Scholar 

  • Žáček P, Kalinova B, Sobotnik J, Hovorka O, Ptacek V, Coppée A, Vereeghen F, 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

    Article  PubMed  Google Scholar 

  • Žáček P, Prchalová-Horňáková D, Tykva R, Kindl J, Vogel H, Svatoš A, Pichová I, Valterová I (2013) De novo biosynthesis of sexual pheromone in the labial gland of bumblebee males. Chembiochem 14:361–371

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Financial support (IV) was provided by the Institute of Organic Chemistry and Biochemistry of the Academy of Sciences of the Czech Republic (#61388963). BM contributed as a PhD student with a grant from the FRS-FNRS (Fonds de la Recherche Scientifique). The authors are particularly grateful to Jean-Christophe Sandoz for all his advice and comments. We acknowledge Elizabeth Curtis for correcting the English.

Author information

Authors and Affiliations

  1. Research Institute of Biosciences, Laboratory of Zoology, University of Mons, Place du Parc 20, 7000, Mons, Belgium

    Nicolas Brasero, Thomas Lecocq, Baptiste Martinet, Roland de Jonghe & Pierre Rasmont

  2. Research Unit Animal and Functionalities of Animal Products (URAFPA), University of Lorraine – INRA, 2 Avenue de la Forêt de Haye, BP 172, 54505, Vandœuvre-lès-Nancy, France

    Thomas Lecocq

  3. Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Flemingovo nám 2, CZ-166 10, Prague, Czech Republic

    Irena Valterová

  4. Faculty of Tropical AgriSciences, Department of Sustainable Technologies, Czech University of Life Sciences, Kamýcká 129, CZ-165 21, Prague, Czech Republic

    Klára Urbanová

Authors
  1. Nicolas Brasero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Lecocq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baptiste Martinet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Irena Valterová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Klára Urbanová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roland de Jonghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pierre Rasmont
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicolas Brasero.

Electronic supplementary material

Supplementary file 1

- Data matrix of cephalic labial gland secretions (CLGS) (relative concentration of each compound), list of the identified compounds, kovats indice and IndVal analysis with specific compounds in Bombus deuteronymus superequester, B. exil, B. filchnerae, B. muscorum and B. humilis subbaicalensis. U indicates undetermined compounds. (XLSX 113 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brasero, N., Lecocq, T., Martinet, B. et al. Variability in Sexual Pheromones Questions their Role in Bumblebee Pre-Mating Recognition System. J Chem Ecol 44, 9–17 (2018). https://doi.org/10.1007/s10886-017-0910-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-017-0910-4

Keywords

Search

Navigation