Arthropod-Plant Interactions

, Volume 1, Issue 2, pp 119–127 | Cite as

Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest

  • Nehal Saleh
  • Alan G. Scott
  • Gareth P. Bryning
  • Lars Chittka
Original Paper


Chemicals used in communication are divided into signals and cues. Signals are moulded by natural selection to carry specific meanings in specific contexts. Cues, on the other hand, have not been moulded by natural selection to carry specific information for intended receivers. Distinguishing between these two modes of information transfer is difficult when animals do not perform obvious secretion behaviours. Although a number of insects have been suspected of leaving cues at food sites and nest entrances, studies have not attempted to experimentally distinguish between cues and signals. Here, we examine the chemical composition of the scent marks left by the bumblebee Bombus terrestris at food sites and compare it to those found at a neutral location. If bees are depositing a cue, we expect the same chemicals to be found at both sites, but if they deposit a signal we only expect to find the scent marks at the food site. We were also interested in identifying the chemicals left at the nest entrance to determine if they differed from those used to mark food sites. We find that bees deposit the same chemicals at food, nest and neutral sites. Therefore, bumblebees leave behind general chemical footprints everywhere they walk and we propose that they learn to use these footprints in a manner that ultimately enhances their fitness, for example, to improve their foraging efficiency and locate their nest. Experimentally, distinguishing these two modes of information transfer is crucial for understanding how they interact to shape animal behaviour and what chemical bouquets are under natural selection.


Chemosensory cue Cuticular hydrocarbons Exocrine gland Foraging Pheromone Trail-laying 



We would like to thank James Logan, Stefan Jarau, Peter Wyatt and Mike Birkett for advice with the GC–MS setup, and Larissa Collins for help with PCA. This study was funded by a Central Research Fund from the University of London to NS.


  1. Ayasse M, Marlovits T, Tengo J, Taghizadeh T, Francke W (1995) Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L. (Hymenoptera, Apidae). Apidologie 26:163–180Google Scholar
  2. Beauchamp GK, Doty RL, Moulton DG (1976) The pheromone concept in mammalian chemical communication: a critique. In: Doty RL (ed) Mammalian olfaction, reproductive processes, and behavior. Academic Press, Inc. Ltd., LondonGoogle Scholar
  3. Butler CG, Fletcher DJC, Walter D (1969) Nest-entrance marking with pheromones by the honeybee-Apis mellifera L., and by the wasp, Vespula vulgaris L. Anim Behav 17:142–147CrossRefGoogle Scholar
  4. Cameron SA (1981) Chemical signals in bumble bee foraging. Behav Ecol Sociobiol 9:257–260CrossRefGoogle Scholar
  5. Carlson DA, Roan CS, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long-chain alkenes, alkadienes, and alkatrienes for gas-chromatography mass-spectrometry. Anal Chem 61:1564–1571CrossRefGoogle Scholar
  6. Cederberg B. (1977) Evidence for trail marking in Bombus terrestris workers (Hymenoptera, Apidae). Zoon 5:143–146Google Scholar
  7. Chittka L, Williams NM, Rasmussen H, Thomson JD (1999) Navigation without vision: bumblebee orientation in complete darkness. Proc R Soc Lond Ser B Biol Sci, 266:45–50CrossRefGoogle Scholar
  8. 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 Senses 30:477–489PubMedCrossRefGoogle Scholar
  9. Dronnet S, Simon X, Verhaeghe JC, Rasmont P, Errard C (2005) Bumblebee inquilinism in Bombus (Fernaldaepsithyrus) sylvestris (Hymenoptera, Apidae): behavioural and chemical analyses of host–parasite interactions. Apidologie 36:59–70CrossRefGoogle Scholar
  10. Eltz T (2006) Tracing pollinator footprints on natural flowers. J Chem Ecol 32:907–915PubMedCrossRefGoogle Scholar
  11. Ferguson AW, Free JB (1979) Production of a forage-marking pheromone by the honeybee. J Apicultural Res 18:128–135Google Scholar
  12. Foster RL, Gamboa GJ (1989) Nest entrance marking with colony specific odors by the bumble bee Bombus occidentalis (Hymenoptera, Apidae). Ethology 81:273–278CrossRefGoogle Scholar
  13. Frisch KV (1967) The dance language and orientation of bees. Harvard University Press, CambridgeGoogle Scholar
  14. Giurfa M, Núñez JA (1992) Honeybees mark with scent and reject recently visited flowers. Oecologia 89:113–117CrossRefGoogle Scholar
  15. Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911CrossRefGoogle Scholar
  16. Granero AM, Sanz JMG, Gonzalez FJE, Vidal JLM, Dornhaus A, Ghani J, Serrano AR, Chittka L (2005) Chemical compounds of the foraging recruitment pheromone in bumblebees. Naturwissenschaften 92:371–374PubMedCrossRefGoogle Scholar
  17. Jandt JM, Curry C, Hemauer S, Jeanne RL (2005) The accumulation of a chemical cue: nest-entrance trail in the German yellowjacket, Vespula germanica. Naturwissenschaften 92:242–245PubMedCrossRefGoogle Scholar
  18. 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 30:793–804PubMedCrossRefGoogle Scholar
  19. Karlson P, Luscher M (1959) Pheromones’: a new term for a class of biologically active substances. Nature 183:55–56PubMedCrossRefGoogle Scholar
  20. Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182CrossRefGoogle Scholar
  21. Oldham NJ, Billen J, Morgan ED (1994) On the similarity of the dufour gland secretion and the cuticular hydrocarbons of some bumblebees. Physiol Entomol 19:115–123Google Scholar
  22. Pouvreau A (1991) Morphology and histology of tarsal glands in bumble bees of the Genera Bombus, Pyrobombus, and Megabombus. Can J Zool 69:866–872CrossRefGoogle Scholar
  23. Pouvreau A (1996) Nest-entrance marking of the bumblebee. Entomol Exp Appl 80:355–364CrossRefGoogle Scholar
  24. Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220CrossRefGoogle Scholar
  25. Saleh N, Ohashi K, Thomson JD, Chittka L (2006) Facultative use of repellent scent mark in foraging bumblebees: complex versus simple flowers. Anim Behav 71:847–854CrossRefGoogle Scholar
  26. Schal C., Sevala VL, Young HP, Bachmann JAS (1998) Sites of synthesis and transport pathways of insect hydrocarbons: cuticle and ovary as target tissues. Am Zool 38:382–393Google Scholar
  27. Schiestl FP, Ayasse M (2000) Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior. Behav Ecol Sociobiol 48:303–307CrossRefGoogle Scholar
  28. Schmitt U, Bertsch A (1990) Do foraging bumblebees scent mark food sources and does it matter. Oecologia 82:137–144CrossRefGoogle Scholar
  29. Schmitt U, Lubke G, Francke W (1991) Tarsal secretion marks food sources in bumblebees (Hymenoptera: Apidae). Chemoecology 2:35–40CrossRefGoogle Scholar
  30. Schmidt VM, Zucchi R, Barth FG (2005) Scent marks left by Nannotrigona testaceicornis at the feeding site: cues rather than signals. Apidologie 36:285–291CrossRefGoogle Scholar
  31. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge, MAGoogle Scholar
  32. Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80Google Scholar
  33. Steinmetz I, Schmolz E, Ruther J (2003) Cuticular lipids as trail pheromone in a social wasp. Proc R Soc Lond Ser B Biol Sci, 270:385–391CrossRefGoogle Scholar
  34. Stout JC, Goulson D (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav Ecol Sociobiol 52:239–246CrossRefGoogle Scholar
  35. Stout JC, Goulson D, Allen JA (1998) Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus spp.). Behav Ecol Sociobiol 43:317–326CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Nehal Saleh
    • 1
  • Alan G. Scott
    • 1
  • Gareth P. Bryning
    • 2
  • Lars Chittka
    • 1
  1. 1.School of Biological and Chemical Sciences, Queen Mary CollegeUniversity of LondonLondonUK
  2. 2.Central Science LaboratorySand Hutton YorkUK

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