Behavioral Ecology and Sociobiology

, Volume 62, Issue 12, pp 1919–1926 | Cite as

Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris

  • Mathieu MoletEmail author
  • Lars Chittka
  • Ralph J. Stelzer
  • Sebastian Streit
  • Nigel E. Raine
Original Paper


Foraging activity in social insects should be regulated by colony nutritional status and food availability, such that both the emission of, and response to, recruitment signals depend on current conditions. Using fully automatic radio-frequency identification (RFID) technology to follow the foraging activity of tagged bumblebees (Bombus terrestris) during 16,000 foraging bouts, we tested whether the cue provided by stored food (the number of full honeypots) could modulate the response of workers to the recruitment pheromone signal. Artificial foraging pheromones were applied to colonies with varied levels of food reserves. The response to recruitment pheromones was stronger in colonies with low food, resulting in more workers becoming active and more foraging bouts being performed. In addition to previous reports showing that in colonies with low food successful foragers perform more excited runs during which they release recruitment pheromone and inactive workers are more prone to leave the nest following nectar influx, our results indicate that evolution has shaped a third pathway that modulates bumblebee foraging activity, thus preventing needless energy expenditure and exposure to risk when food stores are already high. This new feedback loop is intriguing since it involves context-dependent response to a signal. It highlights the integration of information from both forager-released pheromones (signal) and nutritional status (cue) that occurs within individual workers before making the decision to start foraging. Our results support the emerging view that responses to pheromones may be less hardwired than commonly acknowledged.


Activity pattern Context dependence Cue Feedback Honeypot Signal Social insect 



We would like to thank Syngenta Bioline Bees for supplying bumblebee colonies, Oscar Ramos Rodriguez for help with experiments and colony maintenance, and three anonymous referees for useful comments. This work was supported by a grant from the Natural Environment Research Council (NE/F523342/1). The experiments comply with the current laws of the country in which they were performed.

Supplementary material

265_2008_623_MOESM1_ESM.doc (176 kb)
Supplementary Electronic Material (DOC 176 KB)


  1. Beckers R, Deneubourg JL, Goss S (1992) Trail laying behaviour during food recruitment in the ant Lasius niger (L.). Insect Soc 39:59–72CrossRefGoogle Scholar
  2. Billen J (2006) Signal variety and communication in social insects. Proc Neth Entomol Soc Meet 17:9–25Google Scholar
  3. Bishop C (1995) Neural networks for pattern recognition. Oxford University Press, Oxford, UKGoogle Scholar
  4. Cartar RV (1991) Colony energy requirements affect response to predation risk in foraging bumble bees. Ethology 87:90–96CrossRefGoogle Scholar
  5. Cartar RV (1992) Adjustment of foraging effort and task switching in energy-manipulated wild bumblebee colonies. Anim Behav 44:75–87CrossRefGoogle Scholar
  6. Den Boer SPA, Duchateau MJHM (2006) A larval hunger signal in the bumblebee Bombus terrestris. Insect Soc 53:369–373CrossRefGoogle Scholar
  7. Dornhaus A, Chittka L (2005) Bumble bees (Bombus terrestris) store both food and information in honeypots. Behav Ecol 16:661–666CrossRefGoogle Scholar
  8. Dornhaus A, Brockman A, Chittka L (2003) Bumble bees alert to food with pheromone from tergal gland. J Comp Physiol A 189:47–51Google Scholar
  9. Free JB, Butler CG (1959) Bumblebees. MacMillan, New-YorkGoogle Scholar
  10. Goulson D, Hughes WOH, Derwent LC, Stout JC (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273Google Scholar
  11. Grozinger C, Robinson G (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A 193:461–470CrossRefGoogle Scholar
  12. Hölldobler B (1971) Sex pheromone in the ant Xenomyrmex floridanus. J Insect Physiol 17:1497–1499CrossRefGoogle Scholar
  13. Hughes WOH, Goulson D (2001) Polyethism and the importance of context in the alarm reaction of the grass-cutting ant, Atta capiguara. Behav Ecol Sociobiol 49:503–508CrossRefGoogle Scholar
  14. Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940–948CrossRefGoogle Scholar
  15. Josens RB, Roces F (2000) Foraging in the ant Camponotus mus: nectar-intake rate and crop filling depend on colony starvation. J Insect Physiol 46:1103–1110PubMedCrossRefGoogle Scholar
  16. Keeling CI, Slessor KN, Higo HA, Winston ML (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc Natl Acad Sci U S A 100:4486–4491PubMedCrossRefGoogle Scholar
  17. Mena Granero A, Guerra Sanz JM, Egea González FJ, Martínez Vidal JL, Dornhaus A, Ghani J, Roldan Serrano A, Chittka L (2005) Chemical compounds of the foraging recruitment pheromone in bumblebees. Naturwissenschaften 92:371–374CrossRefGoogle Scholar
  18. Neukirch A (1982) Dependence of the life span of the honeybee (Apis mellifera) upon flight performance and energy consumption. J Comp Physiol B 146:35–40CrossRefGoogle Scholar
  19. Pelletier L, McNeil JN (2004) Do bumblebees always forage as much as they could? Insect Soc 51:271–274CrossRefGoogle Scholar
  20. Pouvreau A (1974) Les ennemis des bourdons. II. Organismes affectant les adultes. Apidologie 5:39–62CrossRefGoogle Scholar
  21. Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc B 275:803–808PubMedCrossRefGoogle Scholar
  22. Raubenheimer D, Gäde G (1996) Separating food and water deprivation in locusts: effects on the patterns of consumption, locomotion and growth. Physiol Entomol 21:76–84CrossRefGoogle Scholar
  23. Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220CrossRefGoogle Scholar
  24. Saleh N, Scott AG, Bryning GP, Chittka L (2007) Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest. Arthropod-Plant Interactions 1:119–127CrossRefGoogle Scholar
  25. Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80CrossRefGoogle Scholar
  26. Simpson SJ, Sword GA, Lorch PD, Couzin LD (2006) Cannibal crickets on a forced march for protein and salt. Proc Natl Acad Sci U S A 103:4152–4156PubMedCrossRefGoogle Scholar
  27. Sladen FWL (1912) The Humble-bee. Logaston Press, Woonton, UKGoogle Scholar
  28. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745PubMedCrossRefGoogle Scholar
  29. Smith JM, Harper D (2003) Animal signals. Oxford University Press, Oxford, U.KGoogle Scholar
  30. Stowers L, Marton TF (2005) What is a pheromone? Mammalian pheromones reconsidered. Neuron 46:699–702PubMedCrossRefGoogle Scholar
  31. Streit S, Bock F, Pirk CWW, Tautz J (2003) Automatic life-long monitoring of individual insect behaviour now possible. Zoology 106:169–171PubMedCrossRefGoogle Scholar
  32. Sumner S, Lucas E, Barker J, Isaac N (2007) Radio-tagging technology reveals extreme nest-drifting behavior in a eusocial insect. Curr Biol 17:140–145PubMedCrossRefGoogle Scholar
  33. Velthuis HHW, Van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37:421–451CrossRefGoogle Scholar
  34. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31:389–394CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Mathieu Molet
    • 1
    Email author
  • Lars Chittka
    • 1
  • Ralph J. Stelzer
    • 1
  • Sebastian Streit
    • 2
  • Nigel E. Raine
    • 1
  1. 1.Research Centre for Psychology, School of Biological and Chemical Sciences, Queen MaryUniversity of LondonLondonUK
  2. 2.EDV ConsultingKölnGermany

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