pp 1–11 | Cite as

(S)-2-Heptanol, the alarm pheromone of the stingless bee Melipona solani (Hymenoptera, Meliponini)

  • David Alavez-Rosas
  • Daniel Sánchez-Guillén
  • Edi A. Malo
  • Leopoldo Cruz-LópezEmail author
Original article


Timely defence response is critical in any highly social bee species. Chemical signalling is closely linked to this behaviour, and several pheromones have been discovered. In this work, we identified the pheromone of the stingless bee Melipona solani and evaluated the electrophysiological and behavioural response of the bee to the identified compound. We determined that the mandibular glands serve as the reservoir of the alarm pheromone. Because enantiomeric recognition has been scarcely examined, we performed bioassays and electroantennographic (EAG) studies to determine the role of chirality in pheromone recognition. We found that (S)-2-heptanol was the active compound involved in the alarm response of this species. Although we did not find (R)-2-heptanol in the mandibular gland extracts, bees responded to it in a similar way to the (S)-isomer and to a racemic mixture. The behavioural response of M. solani was flight, different from other Melipona species behaviour. We discuss these findings in an evolutionary and ecological framework.


Alarm pheromone Defence Stingless bees Optical isomerism CG-MS EAG 



We thank Rodrigo López and Bryan Gómez for assistance in the bioassays work.

Funding information

Thanks are given to the National Council of Science and Technology CONACYT for scholarship to D. A. R. (CV/grant number 387462/255265). This study was supported by CONACYT INFR-2014-01(224846).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2019_639_MOESM1_ESM.pdf (115 kb)
ESM 1. (PDF 114 kb)
13592_2019_639_MOESM2_ESM.pdf (127 kb)
ESM 2. (PDF 127 kb)
13592_2019_639_MOESM3_ESM.pdf (43 kb)
ESM 3. (PDF 42 kb)
13592_2019_639_MOESM4_ESM.pdf (34 kb)
ESM 4. (PDF 34 kb)


  1. Alavez-Rosas D, Malo E, Guzmán M, et al (2017) The stingless bee Melipona solani deposits a signature mixture and methyl oleate to mark valuable food sources. J. Chem. Ecol. 43:945–954. CrossRefGoogle Scholar
  2. Amano K, Nemoto T, Heard T (2000) What are stingless bees and why and how to use in crop pollination? A review. Jpn. Agric. Res. Q. 34:183–190.Google Scholar
  3. Ascher J, Pickering J (2017) Discover life: bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Accessed 17 Jul 2017
  4. Ayala R, Gonzalez V, Engel M (2013) Mexican stingless bees (Hymenoptera: Apidae): diversity, distribution, and indigenous knowledge. In: Vit P, Pedro S, Roubik D (eds) Pot-Honey. A legacy of stingless bees, 1st edn. Springer, New York, pp 135–152Google Scholar
  5. Borg-Karlson AK, Tengö J, Valterová I, et al (2003) (S)-(+)-linalool, a mate attractant pheromone component in the bee Colletes cunicularius. J. Chem. Ecol. 29:1–14. CrossRefGoogle Scholar
  6. Breed M, Guzmán-Novoa E, Hunt G (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 49:271–298. CrossRefGoogle Scholar
  7. Cameron E, Franck P, Oldroyd B (2004) Genetic structure of nest aggregations and drone congregations of the southeast Asian stingless bee Trigona collina. Mol. Ecol. 13:2357–2364. CrossRefGoogle Scholar
  8. Cruz-López L, Malo E, Morgan E, et al (2005) Mandibular gland secretion of Melipona beecheii: chemistry and behavior. J. Chem. Ecol. 31:1621–1632. CrossRefGoogle Scholar
  9. Cruz-López L, Aguilar S, Malo E, et al (2007) Electroantennogram and behavioral responses of workers of the stingless bee Oxytrigona mediorufa to mandibular gland volatiles. Entomol. Exp. Appl. 123:43–47. CrossRefGoogle Scholar
  10. Gracioli-Vitti L, Abdalla F, Silva R, Jones G (2004) The chemical composition of the mandibular gland secretion of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Apidae, Meliponini): a comparative study among castes and sexes. J. Braz. Chem. Soc. 15:777–781. CrossRefGoogle Scholar
  11. Grajales-Conesa J, Rojas J, Guzmán-Díaz M, et al (2007) Cephalic and Dufour gland secretions of Scaptotrigona mexicana queens: chemical composition and biological activity. Apidologie 38:38–46. CrossRefGoogle Scholar
  12. Jarau S, Hrncir M, Zucchi R, Barth F (2004) A stingless bee uses labial gland secretions for scent trail communication (Trigona recursa Smith 1863). J. Comp. Physiol. A. 190:233–239. CrossRefGoogle Scholar
  13. Johnson L, Hubbell S (1974) Aggression and competition among stingless bees: field studies. Ecology 55:120–127. CrossRefGoogle Scholar
  14. Johnson L, Wiemer D (1982) Nerol: An alarm substance of the stingless bee, Trigona fulviventris (Hymenoptera: Apidae). J. Chem. Ecol. 8:1167–1181. CrossRefGoogle Scholar
  15. Johnson L, Haynes L, Carlson M, et al (1985) Alarm substances of the stingless bee, Trigona silvestriana. J. Chem. Ecol. 11:409–416. CrossRefGoogle Scholar
  16. Katzav-Gozansky T, Soroker V, Kamer J, et al (2003) Ultrastructural and chemical characterization of egg surface of honeybee worker and queen-laid eggs. Chemoecology 13:129–134. CrossRefGoogle Scholar
  17. Leonhardt S (2017) Chemical ecology of stingless bees. J. Chem. Ecol. 43:385–402. CrossRefGoogle Scholar
  18. Luby J, Regnier F, Clarke E, et al (1973) Volatile cephalic substances of the stingless bees, Trigona mexicana and Trigona pectoralis. J. Insect Physiol. 19:1111–1127. CrossRefGoogle Scholar
  19. Malo E, Castrejón-Gómez V, Cruz-López L, Rojas JC (2004) Antennal sensilla and electrophysiological response of male and female Spodoptera frugiperda (Lepidoptera: Noctuidae) to conspecific sex pheromone and plant odors. Ann. Entomol. Soc. Am. 97:1273–1284.[1273:ASAERO]2.0.CO;2Google Scholar
  20. Meléndez-Ramirez V, Meneses-Calvillo L, Kevan P (2013) Effects of human disturbance and habitat fragmentation on stingless bees. In: Vit P, Pedro S, Roubik D (eds) Pot honey: a legacy of stingless bees, 1st edn. Springer, New York, pp 269–282CrossRefGoogle Scholar
  21. Michener C (2007) The bees of the world, 2nd edn. The Johns Hoptkins University Press, BaltimoreGoogle Scholar
  22. Michener C (2013) The Meliponini. In: Vit P, Silva P, Roubik D (eds) Pot honey: a legacy of stingless bees, 1st edn. Springer-Verlag, New York, pp 3–17CrossRefGoogle Scholar
  23. Mori K (1998) Chirality and insect pheromones. Chirality 10:578–586.<578::AID-CHIR5>3.0.CO;2-Z CrossRefGoogle Scholar
  24. Mori K (2014) Stereochemical studies on pheromonal communications. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 90:373–388. CrossRefGoogle Scholar
  25. Patricio E, Cruz-López L, Morgan E (2004) Electroantennography in the study of two stingless bee species (Hymenoptera: Meliponini). Braz. J. Biol. 64:827–31. CrossRefGoogle Scholar
  26. Pianaro A, Menezes C, Kerr W, et al (2009) Stingless bees: Chemical differences and potential functions in Nannotrigona testaceicornis and Plebeia droryana males and workers. J. Chem. Ecol. 35:1117–1128. CrossRefGoogle Scholar
  27. Plettner E, Lazar J, Prestwich E, Prestwich G (2000) Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar. Biochemistry 39:8953–8962. CrossRefGoogle Scholar
  28. R Core Team (2016) R: A language and environment for statistical computingGoogle Scholar
  29. Ramírez S, Nieh J, Quental T, et al (2010) A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Mol. Phylogenet. Evol. 56:519–525. CrossRefGoogle Scholar
  30. Rochat D, Ramirez-Lucas P, Malosse C, et al (2000) Role of solid-phase microextraction in the identification of highly volatile pheromones of two Rhinoceros beetles Scapanes australis and Strategus aloeus (Coleoptera, Scarabaeidae, Dynastinae). J. Chromatogr. A 885:433–444. CrossRefGoogle Scholar
  31. Roubik D (2006) Stingless bee nesting biology. Apidologie 37:124–143. CrossRefGoogle Scholar
  32. Schorkopf D (2016) Male meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight. J. Comp. Physiol. A. 202:667–678. CrossRefGoogle Scholar
  33. Schorkopf D, Hrncir M, Mateus S, et al (2009) Mandibular gland secretions of meliponine worker bees: further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signalling. J. Exp. Biol. 212:1153–1162. CrossRefGoogle Scholar
  34. Schorkopf D, Mitko L, Eltz T (2011) Enantioselective preference and high antennal sensitivity for (-)-ipsdienol in scent-collecting male orchid bees, Euglossa cyanura. J. Chem. Ecol. 37:953–960. CrossRefGoogle Scholar
  35. Slessor K, Kaminski L, King G, Winston M (1990) Semiochemicals of the honeybee queen mandibular glands. J. Chem. Ecol. 16:851–860. CrossRefGoogle Scholar
  36. Smith B, Roubik D (1983) Mandibular gland of stingless bees (Hymenoptera: Apidae): chemical analysis of their contents and biological function in two species of Melipona. J. Chem. Ecol. 9:1465–1472. CrossRefGoogle Scholar
  37. Strohalm H, Dregus M, Wahl A, Engel K (2007) Enantioselective analysis of secondary alcohols and their esters in purple and yellow passion fruits. J. Agric. Food Chem. 55:10339–10344. CrossRefGoogle Scholar
  38. Tengo J, Agren L, Baur B, et al (1990) Andrena wilkella male bees discriminate between enantiomers of cephalic secretion components. J. Chem. Ecol. 16:429–441. CrossRefGoogle Scholar
  39. Ulland S, Ian E, Borg-Karlson A, Mustaparta H (2006) Discrimination between enantiomers of linalool by olfactory receptor neurons in the cabbage moth Mamestra brassicae (L.). Chem. Senses 31:325–334. CrossRefGoogle Scholar
  40. Vossler F (2012) Flower visits, nesting and nest defence behaviour of stingless bees (Apidae: Meliponini): suitability of the bee species for meliponiculture in the Argentinean Chaco region. Apidologie 43:139–161. CrossRefGoogle Scholar
  41. Wyatt T (2003a) Pheromones and animal behaviour: communications by smell and taste, First. Cambridge University Press, New YorkGoogle Scholar
  42. Wyatt T (2003b) Fight or flight: alarm pheromones. In: Wyatt T (ed) Pheromones and animal behaviour: communications by smell and taste, first. Cambridge University Press, New York, pp 146–163CrossRefGoogle Scholar
  43. Zhang Q, Tolasch T, Schlyter F, Francke W (2002) Enantiospecific antennal response of bark beetles to spiroacetal (E)-conophthorin. J. Chem. Ecol. 28:1839–1852. CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.El Colegio de la Frontera SurTapachulaMexico
  2. 2.Instituto de BiocienciasUniversidad Autónoma de ChiapasTapachulaMexico

Personalised recommendations