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Leg tendon glands in male bumblebees (Bombus terrestris): structure, secretion chemistry, and possible functions

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Abstract

Among the large number of exocrine glands described in bees, the tarsal glands were thought to be the source of footprint scent marks. However, recent studies showed that the compounds used for marking by stingless bees are secreted by leg tendon instead of tarsal glands. Here, we report on the structure of leg tendon glands in males of Bombus terrestris, together with a description of the chemical composition of their secretions and respective changes of both during the males’ lives. The ultrastructure of leg tendon glands shows that the secretory cells are located in three independent regions, separated from each other by unmodified epidermal cells: in the femur, tibia, and basitarsus. Due to the common site of secretion release, the organ is considered a single secretory gland. The secretion of the leg tendon glands of B. terrestris males differs in its composition from those of workers and queens, in particular by (1) having larger proportions of compounds with longer chain lengths, which we identified as wax esters; and (2) by the lack of certain hydrocarbons (especially long chain dienes). Other differences consist in the distribution of double bond positions in the unsaturated hydrocarbons that are predominantly located at position 9 in males but distributed at seven to nine different positions in the female castes. Double bond positions may change chemical and physical properties of a molecule, which can be recognized by the insects and, thus, may serve to convey specific information. The function of male-specific compounds identified from their tendon glands remains elusive, but several possibilities are discussed.

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References

  • Arnhart L (1923) Das Krallenglied der Honigbiene. Arch Bienenkunde 5:37–86

    Google Scholar 

  • Ayasse M, Paxton R, Tengö J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78

    Article  PubMed  CAS  Google Scholar 

  • Baer B, Maile R, Schmid-Hempel P, Morgan ED, Jones GR (2000) Chemistry of a mating plug in bumblebees. J Chem Ecol 26:1869–1875

    Article  CAS  Google Scholar 

  • Baer B, Morgan ED, Schmid-Hempel P (2001) A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. PNAS 98:3926–3928

    Article  PubMed  CAS  Google Scholar 

  • Bergman P, Bergström G (1997) Scent marking, scent origin, and species specificity in male premating behavior of two Scandinavian bumblebees. J Chem Ecol 23:1235–1251

    Article  CAS  Google Scholar 

  • Billen J (2009) Occurrence and structural organization of the exocrine glands in the legs of ants. Arthropod Struct Dev 38:2–15

    Article  PubMed  CAS  Google Scholar 

  • Billen J, Morgan ED (1998) Pheromone communication in social insects: sources and secretions. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview, Boulder, pp 3–33

    Google Scholar 

  • Carlson DA, Roan C-S, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571

    Article  CAS  Google Scholar 

  • Coppée A, Mathy T, Cammaerts M-C, Verheggen FJ, Terzo M, Iserbyt S, Valterová I, Rasmont P (2011) Age-dependent attractivity of males’ sexual pheromones in Bombus terrestris (L.) [Hymenoptera, Apidae]. Chemoecology 21:75–82

    Article  Google Scholar 

  • da Cruz-Landim C, Franco AC (2000) Epithelial bags inside the tibia and femur of males of Centris (Hymenoptera, Anthophoridae): localization and ultrastructure. Rev Bras Entomol 44:97–103

    Google Scholar 

  • da Cruz-Landim C, Franco AC (2001) Light and electron microscopic aspects of glands and pseudoglandular structures in the legs of bees (Hymenoptera, Apinae, Euglossini). Braz J morphol Sci 18:81–90

    Google Scholar 

  • da Cruz-Landim C, de Moraes RLMS, Salles HC, Reginato RD (1998) Note on glands present in Meliponinae (Hymenoptera, Apidae) bees legs. Rev Bras Zool 15:159–165

    Article  Google Scholar 

  • da Cruz-Landim C, Abdalla FC, Gracioli-Vitti LF (2005) Morphological and functional aspects of volatile-producing glands in bees (Hymenoptera: Apidae). Insect Sci 12:467–480

    Article  Google Scholar 

  • Dahl F (1885) Die Fussdrüsen der Insekten. Arch mikrosk Anat 25:236–262

    Article  Google Scholar 

  • Detrain C, Deneubourg J-L (2009) Social cues and adaptive foraging strategies in ants. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 29–51

    Google Scholar 

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

    Google Scholar 

  • Duvoisin N, Baer B, Schmid-Hempel P (1999) Sperm transfer and male competition in a bumblebee. Anim Behav 58:743–749

    Article  PubMed  Google Scholar 

  • Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–94

    Article  PubMed  CAS  Google Scholar 

  • Fawcett DW (1966) The cell. Its organelles and inclusions. Saunders, Philadelphia

    Google Scholar 

  • Federle W, Brainerd EL, McMahon TA, Hölldobler B (2001) Biomechanics of the movable pretarsal adhesive organ in ants and bees. PNAS 98:6215–6220

    Article  PubMed  CAS  Google Scholar 

  • Free JB (1987) Pheromones of social bees. Cornell University Press, Ithaca

    Google Scholar 

  • Giglio A, Ferrero EA, Brandmayr TZ (2005) Ultrastructural identification of the antennal gland complement in Siagona europaea Dejean 1826, a myrmecophagous carabid beetle. Acta Zool 86:195–203

    Article  Google Scholar 

  • Gilbert LE (1976) Postmating female odor in Heliconius butterflies: a male contributed antiaphrodisiac? Science 193:419–420

    Article  PubMed  CAS  Google Scholar 

  • Goulson D (2009) The use of scent marks by foraging bumble bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 251–260

    Chapter  Google Scholar 

  • Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911

    Article  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package or education and data analysis. Palaeontol Electron 4:9, http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Google Scholar 

  • Jarau S (2009) Chemical communication during food exploitation in stingless bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 223–249

    Chapter  Google Scholar 

  • Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804

    Article  PubMed  CAS  Google Scholar 

  • Jarau S, Hrncir M, Zucchi R, Barth FG (2005) Morphology and structure of the tarsal glands of the stingless bee Melipona seminigra. Naturwissenschaften 92:147–150

    Article  PubMed  CAS  Google Scholar 

  • Kindl J, Hovorka O, Urbanová K, Valterová I (1999) Scent marking in male premating behavior of Bombus confuses. J Chem Ecol 25:1489–1500

    Article  CAS  Google Scholar 

  • Kukuk P (1985) Evidence for an antiaphrodisiac in the sweat bee Lasioglossum (Dialictus) zephyrum. Science 227:656–657

    Article  PubMed  CAS  Google Scholar 

  • Kullenberg B, Bergström G, Bringer B, Carlberg B, 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

    Google Scholar 

  • Lensky Y, Cassier P, Finkel A, Delorme-Joulie C, Levinsohn M (1985) The fine structure of the tarsal glands of the honeybee Apis mellifera L. (Hymenoptera). Cell Tissue Res 240:153–158

    Article  Google Scholar 

  • Martin JS, Carruthers JM, Williams PH, Drijfhout FP (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in bumblebees. J Chem Ecol 36:855–863

    Article  PubMed  CAS  Google Scholar 

  • NIST Mass Spec Data Center SES (2008) Mass spectra, 6th edn. National Institute of Standards and Technology, Gaithersburg, http://webbook.nist.gov/chemistry

    Google Scholar 

  • Noirot C, Quennedey A (1974) Fine structure of insect epidermal glands. Annu Rev Entomol 19:61–80

    Article  Google Scholar 

  • Percy-Cunningham JE, MacDonald JA (1987) Biology and ultrastructure of sex pheromone-producing glands. In: Prestwich GD, Blomquist GJ (eds) Pheromone biochemistry. Academic, Orlando, pp 27–69

    Google Scholar 

  • Pouvreau A (1991) Morphology and histology of tarsal glands in bumble bees of the genera Bombus, Pyrobombus, and Megabombus. Can J Zool 69:866–872

    Article  Google Scholar 

  • Reinhard J, Srinivasan MV (2009) The role of scents in honey bee foraging and recruitment. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 165–182

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Sauter A, Brown MJF, Baer B, Schmid-Hempel P (2001) Males of social insects can prevent queens from multiple mating. Proc R Soc Lond B 268:1449–1454

    Article  CAS  Google Scholar 

  • Schmid-Hempel R, Schmid-Hempel P (2000) Female mating frequencies in Bombus spp. from Central Europe. Insect soc 47:36–41

    Article  Google Scholar 

  • Schmitt U, Lübke G, Francke W (1991) Tarsal secretion marks food sources in bumblebees (Hymenoptera: Apidae). Chemoecology 2:35–40

    Article  CAS  Google Scholar 

  • Slaa EJ, Hughes WOH (2009) Local enhancement, local inhibition, eavesdropping, and the parasitism of social insect communication. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC, Boca Raton, pp 147–164

    Chapter  Google Scholar 

  • Šobotník J, Kalinová B, Cahlíková L, Weyda F, Ptáček V, Valterová I (2008) Age-dependent changes in structure and function of the male labial gland in Bombus terrestris. J Insect Physiol 54:204–214

    Article  PubMed  Google Scholar 

  • Stout JC, Goulson D, Allen JA (1998) Repellent scent-marking of flowers by a guild of foraging bumble bees (Bombus spp.). Behav Ecol Sociobiol 43:317–326

    Article  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 

  • Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones—an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514

    Article  PubMed  CAS  Google Scholar 

  • Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. In: Kinne O (ed) Excellence in ecology, book 2. Ecology Institute, Oldendorf/Luhe

    Google Scholar 

  • Žáček P, Kalinová B, Šobotník J, Hovorka O, Ptáček V, Coppée A, Verheggen F, Valterová 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 

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Acknowledgments

This work was financially supported by the Technological Agency of the Czech Republic (project no. TA01020969) and by the Academy of Sciences of the Czech Republic (research project RVO: 61388963). S.J. is supported by a research grant from the German Research Council, DFG (project no. JA 1715/3-1). The authors also wish to thank Alena Bučánková for providing part of the biological material and to the staff of the Laboratory of Electron microscopy (Charles University in Prague) for their help with TEM sample preparation.

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Authors and Affiliations

  1. Institute for Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89081, Ulm, Germany

    Stefan Jarau

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

    Petr Žáček, Jan Šobotník, Vladimír Vrkoslav, Romana Hadravová, Audrey Coppée, Soňa Vašíčková, Pavel Jiroš & Irena Valterová

  3. Department of Analytical Chemistry, Faculty of Science, Charles University, Albertov 8, 128 40, Prague, Czech Republic

    Petr Žáček

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  1. Stefan Jarau
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Correspondence to Jan Šobotník.

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Communicated by: Sven Thatje

Stefan Jarau and Petr Žáček contributed equally to this work.

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Jarau, S., Žáček, P., Šobotník, J. et al. Leg tendon glands in male bumblebees (Bombus terrestris): structure, secretion chemistry, and possible functions. Naturwissenschaften 99, 1039–1049 (2012). https://doi.org/10.1007/s00114-012-0986-1

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