Abstract
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.
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References
Beckers R, Deneubourg JL, Goss S (1992) Trail laying behaviour during food recruitment in the ant Lasius niger (L.). Insect Soc 39:59–72
Billen J (2006) Signal variety and communication in social insects. Proc Neth Entomol Soc Meet 17:9–25
Bishop C (1995) Neural networks for pattern recognition. Oxford University Press, Oxford, UK
Cartar RV (1991) Colony energy requirements affect response to predation risk in foraging bumble bees. Ethology 87:90–96
Cartar RV (1992) Adjustment of foraging effort and task switching in energy-manipulated wild bumblebee colonies. Anim Behav 44:75–87
Den Boer SPA, Duchateau MJHM (2006) A larval hunger signal in the bumblebee Bombus terrestris. Insect Soc 53:369–373
Dornhaus A, Chittka L (2005) Bumble bees (Bombus terrestris) store both food and information in honeypots. Behav Ecol 16:661–666
Dornhaus A, Brockman A, Chittka L (2003) Bumble bees alert to food with pheromone from tergal gland. J Comp Physiol A 189:47–51
Free JB, Butler CG (1959) Bumblebees. MacMillan, New-York
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 130:267–273
Grozinger C, Robinson G (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A 193:461–470
Hölldobler B (1971) Sex pheromone in the ant Xenomyrmex floridanus. J Insect Physiol 17:1497–1499
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 49:503–508
Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940–948
Josens RB, Roces F (2000) Foraging in the ant Camponotus mus: nectar-intake rate and crop filling depend on colony starvation. J Insect Physiol 46:1103–1110
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 100:4486–4491
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 92:371–374
Neukirch A (1982) Dependence of the life span of the honeybee (Apis mellifera) upon flight performance and energy consumption. J Comp Physiol B 146:35–40
Pelletier L, McNeil JN (2004) Do bumblebees always forage as much as they could? Insect Soc 51:271–274
Pouvreau A (1974) Les ennemis des bourdons. II. Organismes affectant les adultes. Apidologie 5:39–62
Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc B 275:803–808
Raubenheimer D, Gäde G (1996) Separating food and water deprivation in locusts: effects on the patterns of consumption, locomotion and growth. Physiol Entomol 21:76–84
Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220
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 1:119–127
Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80
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 103:4152–4156
Sladen FWL (1912) The Humble-bee. Logaston Press, Woonton, UK
Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745
Smith JM, Harper D (2003) Animal signals. Oxford University Press, Oxford, U.K
Stowers L, Marton TF (2005) What is a pheromone? Mammalian pheromones reconsidered. Neuron 46:699–702
Streit S, Bock F, Pirk CWW, Tautz J (2003) Automatic life-long monitoring of individual insect behaviour now possible. Zoology 106:169–171
Sumner S, Lucas E, Barker J, Isaac N (2007) Radio-tagging technology reveals extreme nest-drifting behavior in a eusocial insect. Curr Biol 17:140–145
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 37:421–451
Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol Entomol 31:389–394
Acknowledgments
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.
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Communicated by: M. Beekman
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Molet, M., Chittka, L., Stelzer, R.J. et al. Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris . Behav Ecol Sociobiol 62, 1919–1926 (2008). https://doi.org/10.1007/s00265-008-0623-3
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DOI: https://doi.org/10.1007/s00265-008-0623-3