Behavioral Ecology and Sociobiology

, Volume 66, Issue 2, pp 275–286 | Cite as

An integrated look at decision-making in bees as they abandon a depleted food source

Original Paper


While there has been considerable research on the behavioral processes that underlie animals’ ability respond to shifting rewards, it remains unclear how animals coordinate multiple processes over time. To investigate this, we compared the behavior of honeybees (Apis mellifera) and bumblebees (Bombus impatiens), in an open-ended search task. Bees were given brief access to a high-quality food source, which then became non-rewarding. Then, over an extended period, we examined (1) bees’ tendency to persist at the depleted site, (2) their tendency to return to a different low-quality food source where they had been foraging previously, (3) their tendency to return to the hive, and (4) how previous reward history influenced their tendency to shift among these options. Compared to bumblebees, honeybees were much slower to abandon the depleted site and were much more likely to make trips to the hive while bumblebees were much more likely to return to the familiar low-quality site. These observed species differences are interpreted in terms of evolved individual and social differences between these species. We show evidence of well-studied behavioral processes such as extinction, negative contrast effects, and reliance on a social group, and provide, for the first time, a picture of how these processes interact with one another as part of a common sequential decision-making process.


Foraging behavior Honeybees Bumblebees Sequential decision-making Extinction Negative contrast effects 



We would like to thank our field assistants, Kim Maida, Mara Trudgen, Kourtney Trudgen, Lora Bramlett, Elizabeth Dean, and Jared Ruddick. We would also like to express our gratitude to Randolf Menzel, as well as the two anonymous reviewers, for their comments. Funding was provided by NSF (IGERT DGE 0114378).

Ethical and legal statement

The procedures described above and all care and handing of bees are in full compliance with the institutional guidelines for animal experimentation and with the laws of the United States.

Statement of disclosure

The authors have no financial relationship with the NSF, beyond the funding of the present study. The authors declare no conflict of interest.


  1. Adams-Hunt MM, Jacobs LF (2007) Cognition in foraging. In: Stephens DW, Brown JS, Ydenberg RC (eds) Foraging: behavior and ecology. University of Chicago Press, Chicago, pp 105–138Google Scholar
  2. Baude M, Danchin E, Mugabo M, Dajoz I (2011) Conspecifics as informers and competitors: an experimental study in foraging bumble-bees. P Roy Soc B-Biol Sci 278:2806–2813CrossRefGoogle Scholar
  3. Bitterman ME (1976) Incentive contrast in honey bees. Science 192:380–382PubMedCrossRefGoogle Scholar
  4. Bitterman ME (1996) Comparative analysis of learning in honeybees. Anim Learn Behav 24:123–141CrossRefGoogle Scholar
  5. Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer, Sunderland, MAGoogle Scholar
  6. Bouton ME (1993) Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull 114:80–99PubMedCrossRefGoogle Scholar
  7. Bouton ME (1994) Context, ambiguity, and classical-conditioning. Curr Dir Psychol Sci 3:49–53CrossRefGoogle Scholar
  8. Bouton ME (2002) Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. In. Elsevier, pp 976–986Google Scholar
  9. Bouton ME (2004) Context and behavioral processes in extinction. Learn Memory 11:485–494CrossRefGoogle Scholar
  10. Bouton ME (2007) Learning and behavior: a contemporary synthesis. Sinauer, Sunderland, MAGoogle Scholar
  11. Bouton ME, Westbrook RF, Corcoran KA, Maren S (2006) Contextual and temporal modulation of extinction: behavioral and biological mechanisms. 352–360Google Scholar
  12. Chittka L (1998) Sensorimotor learning in bumblebees: long-term retention and reversal training. J Exp Biol 201:515–524Google Scholar
  13. Couvillon PA, Bitterman ME (1980) Some phenomena of associative learning in honeybees. J Comp Physiol Psych 94:878–885CrossRefGoogle Scholar
  14. Couvillon PA, Bitterman ME (1984) The over-learning extinction effect and successive negative contrast in honeybees (Apis mellifera). J Comp Psychol 98:100–109PubMedCrossRefGoogle Scholar
  15. Cresswell JE (1990) How and why do nectar foraging bumblebees initiate movements between inflorescences of wild bergamot Mondarda fistulosa (Lamiacaea)? Oecologia 82:450–460CrossRefGoogle Scholar
  16. Dechaume-Moncharmont FX, Dornhaus A, Houston AI, McNamara JM, Collins EJ, Franks NR (2005) The hidden cost of information in collective foraging. P Roy Soc B-Biol Sci 272:1689–1695CrossRefGoogle Scholar
  17. Dornhaus A, Chittka L (2001) Food alert in bumblebees (Bombus terrestris): possible mechanisms and evolutionary implications. Behav Ecol Sociobiol 50:570–576CrossRefGoogle Scholar
  18. Dornhaus A, Brockman A, Chittka L (2003) Bumble bees alert to food with pheromone from tergal gland. J Comp Physiol Sensory Neural Behav Physiol 189:47–51Google Scholar
  19. Dyer FC (2002) The biology of the dance language. Annu Rev Entomol 47:917–949PubMedCrossRefGoogle Scholar
  20. Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617–627CrossRefGoogle Scholar
  21. Flaherty CF (1996) Incentive relativity. Cambridge University Press, Cambridge; New YorkGoogle Scholar
  22. Frisch Kv (1993) The dance language and orientation of bees, 1st Harvard University Press pbk. edn. Harvard University Press, Cambridge, Mass.Google Scholar
  23. Galef BG, Yarkovsky N (2009) Further studies of reliance on socially acquired information when foraging in potentially risky situations. Anim Behav 77:1329–1335CrossRefGoogle Scholar
  24. Gibbon J, Fairhurst S, Church RM, Kacelnik A (1988) Scalar expectancy—theory and choice between delayed rewards. Psychol Rev 95:102–114PubMedCrossRefGoogle Scholar
  25. Giraldeau L-A, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton, N.JGoogle Scholar
  26. Giurfa M (1996) Movement patterns of honeybee foragers: motivation and decision rules dependent on the rate of reward. Behaviour 133:579–596CrossRefGoogle Scholar
  27. Glimcher PW (2002) Decisions, decisions, decisions: choosing a biological science of choice. Neuron 36:323–332PubMedCrossRefGoogle Scholar
  28. Greggers U, Menzel R (1993) Memory dynamics and foraging strategies of honeybees. Behav Ecol Sociobiol 32:17–29CrossRefGoogle Scholar
  29. Heinrich B (1979) Bumblebee economics. Harvard University Press, CambridgeGoogle Scholar
  30. Judd TM (1995) The waggle dance of the honeybee—which bees following a dancer successfully acquire the information. J Insect Behav 8:343–354CrossRefGoogle Scholar
  31. Kacelnik A, Bateson M (1996) Risky theories—the effects of variance on foraging decisions. Am Zool 36:402–434Google Scholar
  32. Keasar T, Shmida A, Motro U (1996) Innate movement rules in foraging bees: flight distances are affected by recent rewards and are correlated with choice of flower type. Behav Ecol Sociobiol 39:381–388CrossRefGoogle Scholar
  33. Komischke B, Giurfa M, Lachnit H, Malun D (2002) Successive olfactory reversal learning in honeybees. Learn Memory 9:122–129CrossRefGoogle Scholar
  34. Leadbeater E, Chittka L (2005) A new mode of information transfer in foraging bumblebees? Curr Biol 15:R447–R448PubMedCrossRefGoogle Scholar
  35. Mackintosh NJ (1974) The psychology of animal learning. Academic, LondonGoogle Scholar
  36. Mackintosh NJ (1983) Conditioning and associative learning. Oxford University Press, OxfordGoogle Scholar
  37. Macuda T, Gegear RJ, Laverty TM, Timney B (2001) Behavioural assessment of visual acuity in bumblebees (Bombus impatiens). J Exp Biol 204:559–564PubMedGoogle Scholar
  38. McNamara JM, Webb JN, Collins EJ, Szekely T, Houston AI (1997) A general technique for computing evolutionarily stable strategies based on errors in decision-making. J Theor Biol 189:211–225PubMedCrossRefGoogle Scholar
  39. Menzel R (1969) On honey bees memory of spectral colours (reversal learning and learning of several colours). Z Vergl Physiol 63:290–309CrossRefGoogle Scholar
  40. Menzel R, Greggers U (1992) Temporal dynamics and foraging behaviour in honeybees. In: Billen J (ed) Biology and evolution of social insects. Leuven University Press, Leuven, pp 303–318Google Scholar
  41. Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore, MDGoogle Scholar
  42. Moore D, Van Nest BN, Seier E (2011) Diminishing returns: the influence of experience and environment on time-memory extinction in honey bee foragers. J Comp Physiol A 197:641–651CrossRefGoogle Scholar
  43. Mota T, Giurfa M (2010) Multiple reversal olfactory learning in honeybees. Front Behav Neurosci 4:1–9Google Scholar
  44. Noble J, Todd PM, Tuci E (2001) Explaining social learning of food preferences without aversions: an evolutionary simulation model of Norway rats. P Roy Soc B-Biol Sci 268:141–149CrossRefGoogle Scholar
  45. Nunez JA (1970) The relationship between sugar flow and foraging and recruiting behaviour of honey bees (Apis mellifera L.). Anim Behav 18:527–538CrossRefGoogle Scholar
  46. Nunez JA (1982) Honeybee foraging strategies at a food source in relation to its distance from the hive and the rate of sugar flow. J Apic Res 21:139–150Google Scholar
  47. Page RE, Fondrk MK (1995) The effects of colony level selection on the social-organization of honey-bee (Apis mellifera L.) colonies—colony level components of pollen hoarding. Behav Ecol Sociobiol 36:135–144CrossRefGoogle Scholar
  48. Pavlov IP (1927) Conditioned reflexes. Oxford University Press, Oxford, UKGoogle Scholar
  49. Pecoraro NC, Timberlake WD, Tinsley M (1999) Incentive downshifts evoke search repertoires in rats. J Exp Psychol Anim B 25:153–167CrossRefGoogle Scholar
  50. Pleasants JM, Zimmerman M (1979) Patchiness in the dispersion of nectar resources—evidence for hot and cold spots. Oecologia 41:283–288CrossRefGoogle Scholar
  51. Rescorla R (2001) Experimental Extinction. In: Klein SB, Mowrer RR (eds) Contemporary learning theories—Pavlovian conditioning and the status of traditional learning theory. Erlbaum Associates, Hillsdale, N.J., pp 119–154Google Scholar
  52. Scheiner R, Page RE, Erber J (2001) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem 76:138–150PubMedCrossRefGoogle Scholar
  53. Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142CrossRefGoogle Scholar
  54. Schmitt U, Bertsch A (1990) Do foraging bumblebees scent-mark food sources and does it matter. Oecologia 82:137–144CrossRefGoogle Scholar
  55. Schuck-Paim C, Pompilio L, Kacelnik A (2004) State-dependent decisions cause apparent violations of rationality in animal choice. PLoS Biol 2:2305–2315CrossRefGoogle Scholar
  56. Seeley TD (1983) Division of labor between scouts and recruits in honeybee foraging. Behav Ecol Sociobiol 12:253–259CrossRefGoogle Scholar
  57. Seeley TD (1985) The information-center strategy of honeybee foraging. Forts Zool 31:75–90Google Scholar
  58. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge, MAGoogle Scholar
  59. Seeley TD, Towne WF (1992) Tactics of dance choice in honey-bees—do foragers compare dances. Behav Ecol Sociobiol 30:59–69CrossRefGoogle Scholar
  60. Stephens DW (2008) Decision ecology: foraging and the ecology of animal decision making. Cogn Affect Behav Ne 8:475–484CrossRefGoogle Scholar
  61. Stollhoff N, Eisenhardt D (2009) Consolidation of an extinction memory depends on the unconditioned stimulus magnitude previously experienced during training. J Neurosci 29:9644–9650PubMedCrossRefGoogle Scholar
  62. Sutherland NS, Mackintosh NJ (1971) Mechanisms of animal discrimination learning. Academic, New YorkGoogle Scholar
  63. Towne WF, Gould JL (1988) The spatial precisions of the honey bees' dance communication. J Insect Behav 1:129–155CrossRefGoogle Scholar
  64. Townsend-Mehler JM, Dyer FC, Maida K (2011) Deciding when to explore and when to persist: a comparison of honeybees and bumblebees in their response to downshifts in reward. Behav Ecol Sociobiol 65:305–312CrossRefGoogle Scholar
  65. Warrant E, Porombka T, Kirchner WH (1996) Neural image enhancement allows honeybees to see at night. P Roy Soc B-Biol Sci 263:1521–1526CrossRefGoogle Scholar
  66. Wei CA, Rafalko SL, Dyer FC (2002) Deciding to learn: modulation of learning flights in honeybees, Apis mellifera. J Comp Physiol A 188:725–737CrossRefGoogle Scholar
  67. Wiegmann DD, Wiegmann DA, Waldron FA (2003) Effects of a reward downshift on the consummatory behavior and flower choices of bumblebee foragers. Physiol Behav 79:561–566PubMedCrossRefGoogle Scholar
  68. Worden BD, Papaj DR (2005) Flower choice copying in bumblebees. Biol Lett 1:504–507PubMedCrossRefGoogle Scholar
  69. Zimmerman M (1981) Patchiness in the dispersion of nectar resources—probable causes. Oecologia 49:154–157CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of ZoologyMichigan State UniversityEast LansingUSA

Personalised recommendations