Skip to main content
Log in

The relationship between queen execution and cuticular hydrocarbons in stingless bee Melipona scutellaris (Hymenoptera: Meliponini)

  • Original Article
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

In queenright colonies of stingless bees of the genus Melipona, workers recognize, attack, and kill young virgin queens. For Melipona scutellaris, we observed that virgin queens were executed when they were between 5 and 9 days old, while newly emerged queens were not attacked. The faster movements of old virgin in relation to newly emerged might be responsible for attacks. It has been also hypothesized that cuticular hydrocarbons are the source of the signal used by workers to recognize virgin queens. We investigated whether newly emerged, 8 days old virgin and physogastric queens of M. scutellaris have different cuticular hydrocarbon profiles. Cuticular hydrocarbons of three ages were compared using gas chromatography-mass spectrometry. The cuticular hydrocarbon profiles varied by reproductive status and age. Changes in the cuticular hydrocarbons in virgin queens during aging suggest that these compounds, together with change in movement, may play a role in the recognition of virgin queens by workers prior to regicide.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abdalla FC, Cruz-Landim C (2002) Glândulas exócrinas das abelhas. Funpec, Ribeirão Preto

    Google Scholar 

  • Abdalla FC, Jones GR, Morgan ED, Cruz-Landim C (2003) Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Genet Mol Res 2:191–199

    CAS  PubMed  Google Scholar 

  • Abdalla FC, Jones GR, Morgan ED, Cruz-Landim C (2004) Chemical composition of the Dufour gland secretion in queens of Melipona bicolor (Hymenoptera, Meliponini). J Braz Chem Soc 15:621–625

    Article  CAS  Google Scholar 

  • Amsalem E, Orlova M, Grozinger CM (2015) A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens). Proc R Soc B 282:20151800

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand

  • Biseau JC, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593

    Article  PubMed  Google Scholar 

  • Bonavita-Cougourdan A, Theraulaz G, Bagnères AG, Roux M, Pratte M, Provost E, Clement JL (1991) Cuticular hydrocarbons, social organization and ovarian development in a polistine wasp: Polistes dominulus Christ. Comp Biochem Physiol 100:667–680

    Article  Google Scholar 

  • Caliman MJF (2008) Caracterização do perfil de hidrocarbonetos cuticulares de operárias, rainhas virgens e rainhas fisogástricas de Melipona marginata Lepeletier, 1836 (Hymenoptera, Apinae, Meliponini). Dissertação de Mestrado, Universidade de São Paulo

  • Carlson DA, Offor II, El Messoussi S, Matsuyama K, Mori K, Jallon JM (1998) Sex pheromone of Glossina tachinoides: isolation, identification and synthesis. J Chem Ecol 24:1563–1574

    Article  CAS  Google Scholar 

  • Carlson DA, Geden CJ, Bernier UR (1999) Identification of pupal exuviae of Nasonia vitripennis and Muscidifurax raptorellus parasitoids using cuticular hydrocarbons. Biol Control 15:97–106

    Article  Google Scholar 

  • Chaline N, Sandoz JC, Martin SJ, Ratnieks FL, Jones GR (2005) Learning and discrimination of individual cuticular hydrocarbons by honeybees (Apis mellifera). Chem Sen 30:327–335

    Article  CAS  Google Scholar 

  • Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J Insect Physiol 47:485–493

    Article  CAS  PubMed  Google Scholar 

  • Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Sens 30:477–489

    Article  CAS  Google Scholar 

  • Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2013) Cuticular hydrocarbons mediate discrimination of reproductive and nonreproductive in the ant Myrmecia gulosa. Proc Natl Acad Sci USA 100:10341–10346

    Article  Google Scholar 

  • Elias-Neto M, Nascimento ALO, Bonetti AM, Nascimento FS, Mateus S, Garófalo CA, Bitondi MMG (2013) Heterochrony of cuticular differentiation in eusocial corbiculate bees. Apidologie 45:397–408

    Article  Google Scholar 

  • Engels W, Imperatriz-Fonseca V (1990) Caste development, reproductive strategies, and control of fertility in honey bees and stingless bees. In: Engels W (ed) Social insects: an evolutionary approach to castes and reproduction. Springer, Berlin, pp 167–230

    Chapter  Google Scholar 

  • Everaerts C, Farine J, Cobb M, Ferveur J (2010) Drosophila cuticular hydrocarbons revisited: Mating status alters cuticular profiles. PLoS One 5:e9607

    Article  PubMed  PubMed Central  Google Scholar 

  • Falcon T, Ferreira-Caliman MJ, Nunes FMF, Tanak ED, Nascimento FS, Bitondi MMG (2014) Exoskeleton formation in Apis mellifera: Cuticular hydrocarbons profiles and expression of desaturase and elongase genes during pupal and adult development. Insect Biochem Mol 50:68–81

    Article  CAS  Google Scholar 

  • Ferreira-Caliman MJ, Nascimento FS, Turatti IC, Mateus S, Lopes NP, Zucchi R (2010) The cuticular hydrocarbons profiles in the stingless bee Melipona marginata reflect task-related differences. J Insect Physiol 56:800–804

    Article  CAS  PubMed  Google Scholar 

  • Guerino AC, Cruz-Landim C (2003) Ocorrência e morfologia das glândulas tegumentares do abdome de algumas abelhas (Hymenoptera: Apidae): Um estudo comparado. Neotrop Entomol 32:261–267

    Article  Google Scholar 

  • Hora RR, Ionescu-Hirsh A, Simon T, Delabie J, Robert J, Fresneau D, Hefetz A (2008) Postmating changes in cuticular chemistry and visual appearance in Ectatomma tuberculatum queens (Formicidae: Ectatomminae). Naturwissenschaften 95:55–60

    Article  CAS  PubMed  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioural, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  CAS  PubMed  Google Scholar 

  • Imperatriz-Fonseca VL, Zucchi R (1995) Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie 26:231–244

    Article  Google Scholar 

  • Izzo A, Wells M, Huang Z, Tibbetts E (2010) Cuticular hydrocarbons correlate with fertility, not dominance, in a paper wasp, Polistes dominulus. Behav Ecol Sociobiol 64:857–864

    Article  Google Scholar 

  • Jarau S, Van Veen J, Aguilar I, Ayasse M (2009) Virgin queen execution in the stingless bee Melipona beecheii: the sign stimulus for worder attacks. Apidologie 40:496–507

    Article  Google Scholar 

  • Kather R, Martin SJ (2015) Evolution of cuticular hydrocarbons in the Hymenoptera: A meta-analysis. J Chem Ecol 41:871–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr WE, Zucchi R, Nakadaira JT, Butolo JE (1962) Reproduction in the social bees (Hymenoptera: Apidae). J New York Entomol Soc 70:267–276

    Google Scholar 

  • Kerr WE, Jungnickel H, Morgan ED (2004) Workers of the stingless bee Melipona scutellaris are more similar to males than to queens in their cuticular compounds. Apidologie 35:611–618

    Article  Google Scholar 

  • Kleinert AMP (2005) Colony strength and queen replacement in Melipona marginata (Apidae: Meliponini). Braz J Biol 65:469–476

    Article  Google Scholar 

  • Kleinert AMP, Imperatriz-Fonseca VL (1994) Virgin queen refuges in colonies of Melipona marginata (Apidae, Meliponinae). Braz J Biol 54:247–251

    Google Scholar 

  • Koedam D (1999) Production of queens, workers and males in the stingless bee Melipona favosa (Apidae: Meliponinae): pattern in time and space. Neth J Zool 49:289–302

    Article  Google Scholar 

  • Koedam D, Aguilar MI, Sommeijer MJ (1995) Social interactions of gynes and their longevity in queenright colonies of Melipona favosa (Apidae: Meliponinae). Neth J Zool 45:480–494

    Article  Google Scholar 

  • Legendre P, Legendre L (2003) Numerical ecology, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Harvard University Press, Cambridge

    Google Scholar 

  • Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fen 43:515–530

    Google Scholar 

  • Nelson DR, Dillwith JW, Blomquist GJ (1981) Cuticular hydrocarbons of the house fly, Musca domestica. Insect Biochem 11:187–197

    Article  CAS  Google Scholar 

  • Nunes TM, Turatti ICC, Lopes NP, Zucchi R (2009a) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age and reproductive status. J Chem Ecol 35:1172–1180

    Article  CAS  PubMed  Google Scholar 

  • Nunes TM, Turatti ICC, Mateus S, Nascimento FS, Lopes NP, Zucchi R (2009b) Cuticular hydrocarbon in the stingless bee Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponini): differences between colonies, castes and age. Genet Mol Res 8:589–595

    Article  CAS  PubMed  Google Scholar 

  • Nunes TM, Morgan ED, Drijfhout FP, Zucchi R (2010) Caste-specific cuticular lipids in the stingless bee Friesella schrottkyi. Apidologie 41:579–588

    Article  CAS  Google Scholar 

  • Nunes TM, Mateus S, Favaris AP, Amaral MFZJ, von Zuben LG, Closoki GC, Bento JMS, Oldroyd BP, Silva R, Zucchi R, Silva DB, Lopes NP (2014) Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds. Sci Rep 4:7449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oppelt A, Heinze J (2009) Mating is associated with immediate changes of the hydrocarbon profile of Leptothorax gredleri ant queens. J Insect Physiol 55:624–628

    Article  CAS  PubMed  Google Scholar 

  • Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327

    Article  CAS  Google Scholar 

  • Polerstock AR, Eigenbrode SD, Klowden MJ (2002) Mating alters the cuticular hydrocarbons of female Anopheles gambiae sensu stricto and Aedes aegypti (Diptera: Culidae). J Med Entomol 39:545–552

    Article  CAS  PubMed  Google Scholar 

  • Pomonis JG (1989) Cuticular hydrocarbons of the screwworm, Cochliomyia hominivorax (Diptera: Calliphoridae). Isolation, identification and quantification as a function of age, sex and irradiation. J Chem Ecol 15:2301–2317

    Article  CAS  PubMed  Google Scholar 

  • Sakagami SF, Oniki Y (1963) Behaviour studies of the stingless bees, with special reference to the oviposition process. I Melipona compressipes manaosensis Schwarz J Fac Sci Hokkaido Univ Ser VI Zool 15:300–318

    Google Scholar 

  • Sakagami SF, Montenegro MJ, Kerr WE (1965) Behaviour studies of the stingless bees, with special reference to the oviposition process. V. Melipona quadrifasciata anthidioides Lepeletier. J Fac Sci Hokkaido Univ Ser VI Zool 15:578–607

    Google Scholar 

  • Santos DE, Souza EA, Vieira CU, Zanuncio JC, Serrão JE (2015) Morphology of mandibular and intramandibular glands in workers and virgin queens of Melipona scutellaris. Apidologie 46:23–34

    Article  Google Scholar 

  • Santos-Filho PS, Alves DA, Eterovic A, Imperatriz-Fonseca VL, Kleinert AMP (2006) Numerical investment in sex and caste by stingless bees (Apidae: Meliponini): a comparative analysis. Apidologie 37:207–221

    Article  Google Scholar 

  • Silva DLN, Zucchi R, Kerr WE (1972) Biological and behavioural aspects of the reproduction in some species of Melipona (Hymenoptera, Apidae, Meliponinae). Anim Behav 20:123–132

    Article  PubMed  Google Scholar 

  • Sommeijer MJ, De Bruijn LLM, Meeuwsen FJAJ, Martens EP (2003) Natural patterns of caste and sex allocation in the stingless bees Melipona favosa and M. trinitalis related to worker behavior. Insect Soc 50:38–44

    Article  Google Scholar 

  • Sousa CS, Serrão JE, Bonetti AM, Amaral IMR, Kerr WE, Maranhão AQ, Ueira-Vieira C (2013) Insights into the Melipona scutellaris (Hymenoptera, Apidae, Meliponini) fat body transcriptome. Gen Mol Biol 36:292–297

    Article  Google Scholar 

  • Van Den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr A 11:463–471

    Article  Google Scholar 

  • Van Oystaeyen A, Oliveira RC, Homan L, van Zweden JS, Romero C, Oi CA, d’Ettorre P, Khalesi M, Billen J, Wäckers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290

    Article  PubMed  Google Scholar 

  • Van Veen JW, Sommeijer MJ, Aguilar MI (1999) Behavioural development and abdomen inflation of gynes and newly mated queens of Melipona beecheii (Apidae, Meliponinae). Insect Soc 46:361–365

    Article  Google Scholar 

  • Wenseleers T, Hart AG, Ratnieks FLW, Quezada-Euàn JJG (2004) Queen execution and caste conflict in the stingless bee Melipona beecheii. Ethology 110:725–736

    Article  Google Scholar 

  • Will S, Delabie JHC, Heinze J, Ruther J, Oetller J (2012) Cuticular lipid profiles of fertile and non-fertile Cardiocondyla ant queens. J Insect Physiol 58:1245–1249

    Article  CAS  PubMed  Google Scholar 

  • Wossler TC, Jones GE, Allsopp MH, Hepburn R (2006) Virgin queen mandibular gland signals of Apis mellifera capensis change with age and affect honeybee worker responses. J Chem Ecol 32:1043–1056

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants of Fundação de Amparo à Pesquisa de Minas Gerais-PRONEX EDT #522/07 for JES, and Fundação de Amparo à Pesquisa do Estado de São Paulo #2011-17708-0 and Conselho Nacional de Pesquisa #306103-2013-3 for JRT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edmilson Amaral de Souza.

Additional information

Handling Editor: Günther Raspotnig.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Souza, E.A., Trigo, J.R., Santos, D.E. et al. The relationship between queen execution and cuticular hydrocarbons in stingless bee Melipona scutellaris (Hymenoptera: Meliponini). Chemoecology 27, 25–32 (2017). https://doi.org/10.1007/s00049-016-0226-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-016-0226-9

Keywords

Navigation