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Honeybee cognition

  • Mario Pahl
  • Jürgen Tautz
  • Shaowu Zhang

Abstract

Behavioural research on honeybees has shown that bees are not the simple, hardwired creatures they were once believed to be. Bees display perceptual and ‘cognitive’ abilities that are rich, complex and flexible. In this chapter, we begin a review of these abilities with a brief introduction of the bee’s sensory equipment. Next, we describe several experimental approaches to bee behaviour. As this review is not intended to be exhaustive, we focus on behavioural experiments on free-flying honeybees. The studies described here investigate complex forms of learning and navigation, and mark important steps in understanding the processes underlying the bee’s remarkable behaviours.

Keywords

Comparison Stimulus Transfer Test Sample Stimulus Waggle Dance Proboscis Extension Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107-119PubMedCrossRefGoogle Scholar
  2. Blough DS (1959) Delayed matching in the pigeon. J Exp Anal Behav 2:151-160PubMedCrossRefGoogle Scholar
  3. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege H-C, Menzel R (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1-19PubMedCrossRefGoogle Scholar
  4. Brannon EM, Terrace HS (2000) Representation of the numerosities 1-9 by rhesus macaques (Macaca mulatta). J Exp Psychol Anim Behav Process 26:31-49PubMedCrossRefGoogle Scholar
  5. Cartwright BA, Collett TS (1983) Landmark learning in bees – experiments and models. J Comp Physiol A 151:521-543CrossRefGoogle Scholar
  6. Cheng K (2005) Context cues eliminate retroactive interference effects in honeybees (Apis mellifera). J Exp Biol 208:1019-1024PubMedCrossRefGoogle Scholar
  7. Chittka L, Geiger K (1995) Can honey bees count landmarks? Anim Behav 49:159-164CrossRefGoogle Scholar
  8. Chittka L, Tautz J (2003) The spectral input to honeybee visual odometry. J Exp Biol 206:2393-2397PubMedCrossRefGoogle Scholar
  9. Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vision Res 34:1489-1508PubMedCrossRefGoogle Scholar
  10. Chittka L, Geiger K, Kunze J (1995a) The influences of landmarks on distance estimation of honey bees. Anim Behav 50:23-31CrossRefGoogle Scholar
  11. Chittka L, Kunze J, Shipman C, Buchmann SL (1995b) The significance of landmarks for path integration in homing honeybee foragers. Naturwissenschaften 82:341-343CrossRefGoogle Scholar
  12. Chittka L, Gumbert A, Kunze J (1997) Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behav Ecol 8:239-249CrossRefGoogle Scholar
  13. Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361-377CrossRefGoogle Scholar
  14. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272-274PubMedCrossRefGoogle Scholar
  15. Colborn M, Ahmad-Annuar A, Fauria K, Collett TS (1999) Contextual modulation of visuomotor associations in bumble-bees (Bombus terrestris). Proc R Soc Lond B 266:2413-2418CrossRefGoogle Scholar
  16. Collett TS, Baron J (1994) Biological compasses and the coordinate frame of landmark memories in honeybees. Nature 368:137-140CrossRefGoogle Scholar
  17. Collett TS, Cartwright BA (1983) Eidetic images in insects: their role in navigation. Trends Neurosci 6:101-105CrossRefGoogle Scholar
  18. Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542-552PubMedCrossRefGoogle Scholar
  19. Collett TS, Kelber A (1988) The retrieval of visuo-spatial memories by honeybees. J Comp Physiol A 163:145-150PubMedCrossRefGoogle Scholar
  20. Dacke M, Srinivasan MV (2008) Evidence for counting in insects. Anim Cogn 11:683-689PubMedCrossRefGoogle Scholar
  21. Dale RH (1988) Spacial memory in pigeons on a four-arm radial maze. Can J Psychol 42:78-83PubMedCrossRefGoogle Scholar
  22. Dale K, Harland DP, Manning-Jones A, Collett TS (2005) Weak and strong priming cues in bumblebee contextual learning. J Exp Psychol 208:65-74Google Scholar
  23. D’Amato MR, Salmon DP, Colombo M (1985) Extent and limits of the matching concept in monkeys (Cebus apella). J Exp Psychol Anim Behav Process 11:35-51PubMedCrossRefGoogle Scholar
  24. Davis H (1984) Discrimination of the number three by a raccoon (Procyon lotor). Anim Learn Behav 12:409-413CrossRefGoogle Scholar
  25. Deisig N, Lachnit H, Giurfa M, Hellstern F (2001) Configural olfactory learning in honeybees: negative and positive patterning discrimination. Learn Mem 8:70-78PubMedCrossRefGoogle Scholar
  26. Dyer AG, Neumeyer C, Chittka L (2005) Honeybee (Apis mellifera) vision can discriminate between and recognise images of human faces. J Exp Biol 208:4709-4714PubMedCrossRefGoogle Scholar
  27. Dyer AG, Rosa MGP, Reser DH (2008) Honeybees can recognise images of complex natural scenes for use as potential landmarks. J Exp Biol 211:1180-1186PubMedCrossRefGoogle Scholar
  28. Esch HE, Burns JE (1995) Honeybees use optic flow to measure the distance to a food source. Naturwissenschaften 82:38-40CrossRefGoogle Scholar
  29. Fauria K, Dale K, Colborn M, Collett TS (2002) Learning speed and contextual isolation in bumblebees. J Exp Biol 205:1009-1018PubMedGoogle Scholar
  30. Fuchs S, Kralj J, Tautz J (2006) Radio frequency identification tags (RFID) for monitoring of worker bees infested with Varroa destructor or with Nosema apis at the hive entrance. Apidologie 37:643-645Google Scholar
  31. Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726-735PubMedCrossRefGoogle Scholar
  32. Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801-824CrossRefGoogle Scholar
  33. Giurfa M, Malun D (2004) Associative mechanosensory conditioning of the proboscis extension reflex in honeybees. Learn Mem 11:294-302PubMedCrossRefGoogle Scholar
  34. Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458-461PubMedCrossRefGoogle Scholar
  35. Giurfa M, Zhang SW, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930-933PubMedCrossRefGoogle Scholar
  36. Gould JL (1987) Honey bees store learned flower-landing behaviour according to the time of day. Anim Behav 35:1579-1581CrossRefGoogle Scholar
  37. Gross HJ, Pahl M, Si A, Zhu H, Tautz J, Zhang SW (2009) Number-based visual generalisation in the honeybee. PLoS ONE 4:e4263, doi:10.1371/journal.pone.0004263CrossRefGoogle Scholar
  38. Hellstern F, Wüstenberg D, Hammer M (1995) Contextual learning in honeybees under laboratory conditions. In: Elsner N, Menzel R (eds) Learning and Memory. Proceedings of the 23rd Göttingen Neurobiology Conference. Vol. I. Thieme Verlag, Stuttgart, abstract 30Google Scholar
  39. Herman LM, Gordon JA (1974) Auditory delayed matching in the bottlenose dolphin. J Exp Anal Behav 21:19-26PubMedCrossRefGoogle Scholar
  40. Horridge GA (1996) The honeybee (Apis mellifera) detects bilateral symmetry and discriminates its axis. J Insect Physiol 42:755-764CrossRefGoogle Scholar
  41. Horridge GA, Zhang SW (1995) Pattern vision in honeybees (Apis mellifera): flower-like patterns with no predominant orientation. J Insect Physiol 41:681-688CrossRefGoogle Scholar
  42. Horridge GA, Zhang SW, Lehrer M (1992) Bees can combine range and visual angle to estimate absolute size. Philos Trans R Soc Lond B 337:49-57CrossRefGoogle Scholar
  43. Hu S, Dilcher DL, Jarzen DM, Taylor DW (2008) Early steps of angiospermpollinator coevolution. Proc Natl Acad Sci USA 105:240-245PubMedCrossRefGoogle Scholar
  44. Hunt S, Low J, Burns KC (2008) Adaptive numerical competency in a foodhoarding songbird. Proc R Soc Lond B 275:2373-2379CrossRefGoogle Scholar
  45. Johnson DL, Wenner AM (1966) A relationship between conditioning and communication in honey bees. Anim Behav 14:261-265PubMedCrossRefGoogle Scholar
  46. Judd SPD, Collett TS (1998) Multiple stored views and landmark guidance in ants. Nature 392:710-714CrossRefGoogle Scholar
  47. Keller FS, Schoenfeld WN (1950) Principles of Psychology. Appleton-Century-Crofts, New YorkGoogle Scholar
  48. Kilian A, Yaman S, von Fersen L, Güntürkün O (2003) A bottlenose dolphin discriminates visual stimuli differing in numerosity. Learni Behav 31:133-142CrossRefGoogle Scholar
  49. Konorski J (1959) A new method of physiological investigation of recent memory in animals. Bull Acad Pol Sci Biol 7:115-117Google Scholar
  50. Lehrer M, Srinivasan MV, Zhang SW (1990) Visual edge detection in the honeybee and its chromatic properties. Proc R Soc Lond B 238:321-330CrossRefGoogle Scholar
  51. Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV (2006) Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 16:1471-1476PubMedCrossRefGoogle Scholar
  52. Maleszka R, Helliwell P (2001) Effect of juvenile hormone on short-term olfactory memory in young honeybees (Apis mellifera). Horm Behav 40:403-408PubMedCrossRefGoogle Scholar
  53. Menzel R, Blakers M (1976) Colour receptors in the bee eye – morphology and spectral sensitivity. J Comp Physiol A 108:11-13CrossRefGoogle Scholar
  54. Menzel R, Mueller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379-404PubMedCrossRefGoogle Scholar
  55. Menzel R, Greggers U, Smith A, Berger S, Brandt R, Brunke S, Bundrock G, Hülse S, Plümpe T, Schaupp F, Schüttler E, Stach S, Stindt J, Stollhoff N, Watzl S (2005) Honey bees navigate according to a map-like spatial memory. Proc Natl Acad Sci USA 102:3040-3045PubMedCrossRefGoogle Scholar
  56. Pahl M, Zhu H, Pix W, Tautz J, Zhang SW (2007) Circadian timed episodic-like memory – a bee knows what to do when, and also where. J Exp Biol 210:3559-3567PubMedCrossRefGoogle Scholar
  57. Pick CG, Yanai J (1983) Eight arm maze for mice. Int J Neurosci 21:63-66PubMedCrossRefGoogle Scholar
  58. Prabhu C, Cheng K (2008a) One day is all it takes: circadian modulation of the retrieval of colour memories in honeybees. Behav Ecol Sociobiol 63:11-22CrossRefGoogle Scholar
  59. Prabhu C, Cheng K (2008b) Recency preference of odour memory retrieval in honeybees. Behav Ecol Sociobiol 63:23-32CrossRefGoogle Scholar
  60. Prete FR (2004) Complex Worlds from Simpler Nervous Systems. MIT Press, Cambridge/MAGoogle Scholar
  61. Ratnieks FLW, Wenseleers T (2008) Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol Evol 23:45-52PubMedCrossRefGoogle Scholar
  62. Reinhard J, Srinivasan MV, Guez D, Zhang SW (2004a) Floral scents induce recall of navigational and visual memories in honeybees. J Exp Biol 207:4371-4381CrossRefGoogle Scholar
  63. Reinhard J, Srinivasan MV, Zhang SW (2004b) Olfaction: scent-triggered navigation in honeybees. Nature 427:411CrossRefGoogle Scholar
  64. Reynolds AM, Smith AD, Reynolds DR, Carreck NL, Osborne JL (2007) Honeybees perform optimal scale-free searching flights when attempting to locate a food source. J Exp Biol 210:3763-3770PubMedCrossRefGoogle Scholar
  65. Roberts WA (1972) Short-term memory in pigeon: effects of repetition and spacing. J Exp Psychol 94:74-83CrossRefGoogle Scholar
  66. Ronacher B (1992) Pattern-recognition in honeybees: multidimensional-scaling reveals a city-block metric. Vision Res 32:1837-1843PubMedCrossRefGoogle Scholar
  67. Rossel S, Wehner R (1986) Polarization vision in bees. Nature 323:128-131CrossRefGoogle Scholar
  68. Seeley TD (1995) The Wisdom of the Hive. The Social Physiology of Honey Bee Colonies. Harvard University Press, Cambridge/MAGoogle Scholar
  69. Shettleworth SJ (1998) Cognition, Evolution, and Behavior. Oxford University Press, New YorkGoogle Scholar
  70. Skorupski P, Chittka L (2006) Animal cognition: an insect’s sense of time? Curr Biol 16:R851-R853PubMedCrossRefGoogle Scholar
  71. Srinivasan MV, Lehrer M (1988) Spatial acuity of honeybee vision and its spectral properties. J Comp Physiol A 162:159-172CrossRefGoogle Scholar
  72. Srinivasan MV, Zhang SW, Bidwell NJ (1997) Visually mediated odometry in honeybees. J Exp Biol 200:2513-2522PubMedGoogle Scholar
  73. Srinivasan MV, Zhang SW, Zhu H (1998) Honeybees link sights to smells. Nature 396:637-638CrossRefGoogle Scholar
  74. Srinivasan MV, Poteser M, Kral K (1999) Motion detection in insect orientation and navigation. Vision Res 39:2749-2766PubMedCrossRefGoogle Scholar
  75. Srinivasan MV, Zhang SW, Altwein M, Tautz J (2000) Honeybee navigation: nature and calibration of the ‘odometer’. Science 287:851-853PubMedCrossRefGoogle Scholar
  76. Streit S, Bock F, Pirk CWW, Tautz J (2003) Automatic life-long monitoring of individual insect behaviour now possible. Zoology 106:169-171PubMedCrossRefGoogle Scholar
  77. Su S, Cai F, Si A, Zhang SW, Tautz J, Chen S (2008) East learns from West: Asiatic honeybees can understand dance language of European honeybees. PLoS ONE 3:e2365. doi:10.1371/journal.pone.0002365PubMedGoogle Scholar
  78. Tautz J (2008) The Buzz about Bees: Biology of a Superorganism. Springer, BerlinCrossRefGoogle Scholar
  79. Troje NF, Huber L, Loidolt M, Aust U, Fieder M (1999) Categorical learning in pigeons: the role of texture and shape in complex static stimuli. Vision Res 39:353-366PubMedCrossRefGoogle Scholar
  80. Uller C, Jaeger R, Guidry G, Martin C (2003) Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian. Anim Cogn 6:105-112PubMedGoogle Scholar
  81. van Hateren JH, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 167:649-654CrossRefGoogle Scholar
  82. Vareschi E (1971) Duftunterscheidung bei der Honigbiene – Einzelzell-Ableitungen und Verhaltensreaktionen. Z Vergl Physiol 75:143-173Google Scholar
  83. von Frisch K (1967) The Dance Language and Orientation of Bees. Harvard University Press, Cambridge/MAGoogle Scholar
  84. Wasserman EA (1993) Comparative cognition: beginning the second century of the study of animal intelligence. Psychol Bull 113:211-228CrossRefGoogle Scholar
  85. Wehner R (2001) Polarization vision – a uniform sensory capacity? J Exp Biol 204:2589-2596PubMedGoogle Scholar
  86. Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579-588CrossRefGoogle Scholar
  87. Wehner R, Bleuler S, Nievergelt C, Shah D (1990) Bees navigate by using vectors and routes rather than maps. Naturwissenschaften 77:479-482CrossRefGoogle Scholar
  88. Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129-140PubMedGoogle Scholar
  89. Williams RW, Herrup K (1988) The control of neuron number. Annu Rev Neurosci 11:423-453PubMedCrossRefGoogle Scholar
  90. Witthöft W (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Zoomorphology 61:160-184Google Scholar
  91. Wray MK, Klein BA, Mattila HR, Seeley TD (2008) Honeybees do not reject dances for ‘implausible’ locations: reconsidering the evidence for cognitive maps in insects. Anim Behav 76:261-269CrossRefGoogle Scholar
  92. Zhang SW (2006) Learning of abstract concepts and rules by the honeybee. Int J Comp Psychol 19:318-341Google Scholar
  93. Zhang SW, Srinivasan MV (1994) Prior experience enhances pattern discrimination in insect vision. Nature 368:330-332CrossRefGoogle Scholar
  94. Zhang SW, Srinivasan MV (2004a) Exploration of cognitive capacity in honeybees: higher functions emerge from a small brain. In: Prete FR (ed) Complex Worlds from Simpler Nervous Systems. MIT Press, Cambridge/MA, pp 41-74Google Scholar
  95. Zhang SW, Srinivasan MV (2004b) Visual Perception and Cognition in Honeybees. In: Chalupa LM, Werner JS (eds) The Visual Neurosciences. MIT Press, Cambridge/MA, pp 1501-1513Google Scholar
  96. Zhang SW, Bartsch K, Srinivasan MV (1996) Maze learning by honeybees. Neurobiol Learn Mem 66:267-282PubMedCrossRefGoogle Scholar
  97. Zhang SW, Lehrer M, Srinivasan MV (1999) Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol Learn Mem 72:180-201PubMedCrossRefGoogle Scholar
  98. Zhang SW, Srinivasan MV, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289-3298PubMedCrossRefGoogle Scholar
  99. Zhang SW, Bock F, Si A, Tautz J, Srinivasan MV (2005) Visual working memory in decision making by honey bees. Proc Natl Acad Sci USA 102:5250-5255PubMedCrossRefGoogle Scholar
  100. Zhang SW, Schwarz S, Pahl M, Zhu H, Tautz J (2006) Honeybee memory: a honeybee knows what to do and when. J Exp Biol 209:4420-4428PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Mario Pahl
    • 1
  • Jürgen Tautz
    • 1
  • Shaowu Zhang
    • 2
  1. 1.BEEgroup, BiocenterWürzburg UniversityWürzburgGermany
  2. 2.Visual Sciences GroupResearch School of BiologyCanberraAustralia

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