Abstract
Foraging honeybees find their way from their hive to their food in a stereotypical manner using up to four place-finding servomechanisms in sequence: (1) They first fly a vector (straight-line distance and direction) from their home to the vicinity of the target. Direction is determined by the sun compass and by distant landmarks, while distance is estimated by visual flow. (2) They then beacon in on a landmark near the target location. (3) En route toward the landmark, they may adopt a sensorimotor trajectory that takes them toward the target. (4) Near the expected target location, they attempt image matching, which involves trying to put surrounding landmarks at the correct positions on their eyes. In doing image matching, they fly facing a stereotypical direction, a strategy that makes it unnecessary to translate retinal coordinates into another coordinate system.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Backhaus, W. (1991). Color opponent coding in the visual system of the honeybee.Vision Research,31, 1381–1397.
Becker, L. (1958). Untersuchungen über das Heimfindevermögen der Bienen [Investigations of the homefinding ability in bees].Zeitschrift der Vergleichlichen Physiologie,41, 1–25.
Bennett, A. D. T. (1993). Spatial memory in a food storing corvid. I. Near tall landmarks are primarily used.Journal of Comparative Physiology A,173, 193–207.
Bitterman, M. E. (1996). Comparative analysis of learning in honeybees.Animal Learning & Behavior,24, 123–141.
Brown, M. F., &Demas, G. E. (1994). Evidence for spatial working memory in honeybees (Apis mellifera).Journal of Comparative Psychology,108, 344–352.
Brown, M. F., McKeon, D., Curley, T., Weston, B., Lambert, C., &Lebowitz, B. (1998). Working memory for color in honeybees.Animal Learning & Behavior,26, 264–271.
Brown, M. F., Moore, J. A., Brown, C. H., &Langheld, K. D. (1997). The existence and extent of spatial working memory ability in honeybees.Animal Learning & Behavior,25, 473–484.
Burmeister, S., Couvillon, P. A., &Bitterman, M. E. (1995). Performance of honeybees in analogues of the rodent radial maze.Animal Learning & Behavior,23, 369–375.
Capaldi, E. A., Robinson, G. E., &Fahrbach, S. E. (1999). Neuroethology of spatial learning: The birds and the bees.Annual Review of Psychology,50, 651–682.
Cartwright, B. A., &Collett, T. S. (1979). How honeybees know their distance from a nearby landmark.Journal of Experimental Biology,82, 367–372.
Cartwright, B. A., &Collett, T. S. (1982). How honeybees use landmarks to guide their return to a food source.Nature,295, 560–564.
Cartwright, B. A., &Collett, T. S. (1983). Landmark learning in bees.Journal of Comparative Physiology A,151, 521–543.
Cheng, K. (1986). A purely geometric module in the rat’s spatial representation.Cognition,23, 149–178.
Cheng, K. (1989). The vector sum model of pigeon landmark use.Journal of Experimental Psychology: Animal Behavior Processes,15, 366–375.
Cheng, K. (1994). The determination of direction in landmark-based spatial search in pigeons: A further test of the vector sum model.Animal Learning & Behavior,22, 291–301.
Cheng, K. (1995). Landmark-based spatial memory in the pigeon. In D. L. Medin (Ed.),The psychology of learning and motivation (Vol. 33, pp. 1–21). New York: Academic Press.
Cheng, K. (1998a). Distances and directions are computed separately by honeybees in landmark-based search.Animal Learning & Behavior,26, 455–468.
Cheng, K. (1998b). Honeybees (Apis mellifera) remember two neartarget landmark constellations.Learning & Motivation,29, 435–443.
Cheng, K. (1999a). Landmark-based spatial search in honeybees: I. Use of elements and interlandmark angles.Animal Cognition,2, 73–78.
Cheng, K. (1999b). Landmark-based spatial search in honeybees: II. Using gaps and blocks.Animal Cognition,2, 79–90.
Cheng, K. (1999c). Spatial generalization in honeybees confirms Shepard’s law.Behavioural Processes,44, 309–316.
Cheng, K. (in press). Shepard’s law supported by honeybees in spatial generalization.Psychological Science.
Cheng, K., Collett, T. S., Pickhard, A., &Wehner, R. (1987). The use of visual landmarks by honeybees: Bees weight landmarks according to their distance from the goal.Journal of Comparative Physiology A,161, 469–475.
Cheng, K., Collett, T. S., &Wehner, R. (1986). Honeybees learn the colour of landmarks.Journal of Comparative Physiology A,159, 69–73.
Cheng, K., &Miceli, P. (1996). Modelling timing performance on the peak procedure.Behavioural Processes,37, 137–156.
Cheng, K., &Spetch, M. L. (1998). Mechanisms of landmark use in mammals and birds. In S. Healy (Ed.),Spatial representation in animals (pp. 1–17). Oxford: Oxford University Press.
Cheng, K., Srinivasan, M. V., &Zhang, S. W. (1999). Error is proportional to distance measured by honeybees: Weber’s law in the odometer.Animal Cognition,2, 11–16.
Chittka, L., &Geiger, K. (1995). Honeybee long-distance orientation in a controlled environment.Ethology,99, 117–126.
Church, R. M., Meck, W. H., &Gibbon, J. (1994). Application of scalar timing theory to individual trials.Journal of Experimental Psychology: Animal Behavior Processes,20, 135–155.
Collett, T. S. (1992). Landmark learning and guidance in insects.Philosophical Transactions of the Royal Society of London: Series B,337, 295–303.
Collett, T. S. (1995). Making learning easy: The acquisition of visual information during the orientation flights of social wasps.Journal of Comparative Physiology A,177, 737–747.
Collett, T. S., &Baron, J. (1994). Biological compasses and the coordinate frame of landmark memories in honeybees.Nature,368, 137–140.
Collett, T. S., &Baron, J. (1995). Learnt sensori-motor mappings in honeybees: Interpolation and its possible relevance to navigation.Journal of Comparative Physiology A,177, 287–298.
Collett, T. S., Baron, J., &Sellen, K. (1996). On the encoding of movement vectors by honeybees: Are distance and direction represented independently?Journal of Comparative Physiology A,179, 395–406.
Collett, T. S., Fauria, K., Dale, K., &Baron, J. (1997). Places and patterns-A study of context learning in honeybees.Journal of Comparative Physiology A,181, 343–353.
Collett, T. S., &Kelber, A. (1988). The retrieval of visuo-spatial memories by honeybees.Journal of Comparative Physiology A,163, 145–150.
Collett, T. S., &Rees, J. A. (1997). View-based navigation in Hymenoptera: Multiple strategies of landmark guidance in approach to a feeder.Journal of Comparative Physiology A,181, 47–58.
Collett, T. S., &Zeil, J. (1996). Flights of learning.Current Directions in Psychological Science,5, 149–155.
Collett, T. S., &Zeil, J. (1998). Places and landmarks: An arthropod perspective. In S. Healy (Ed.),Spatial representation in animals (pp. 18–53). Oxford: Oxford University Press.
Couvillon, P. A., Arincorayan, N. M., &Bitterman, M. E. (1998). Control of performance by short-term memory in honeybees.Animal Learning & Behavior,26, 469–474.
Couvillon, P. A., Leiato, T. G., &Bitterman, M. E. (1991). Learning by honeybees (Apis mellifera) on arrival at and departure from a feeding place.Journal of Comparative Psychology,105, 177–184.
Demas, G. E., &Brown, M. F. (1995). Honeybees are predisposed to win-shift but can learn to win-stay.Animal Behaviour,50, 1041–1045.
Dyer, F. C. (1991). Bees acquire route-based memories but not cognitive maps in a familiar landscape.Animal Behaviour,41, 239–246.
Dyer, F. C. (1996). Spatial memory and navigation by honeybees on the scale of the foraging range.Journal of Experimental Biology,199, 147–154.
Dyer, F. C., &Dickinson, J. A. (1994). Development of sun compensation by honey bees: How partially experienced bees estimate the sun’s course.Proceedings of the National Academy of Science,91, 4471–4474.
Dyer, F. C., &Dickinson, J. A. (1996). Sun-compass learning in insects: Representation in a simple mind.Current Directions in Psychological Science,5, 67–72.
Dyer, F. C., &Gould, J. L. (1983). Honey bee navigation.American Scientist,71, 587–597.
Esch, H. E., &Burns, J. E. (1995). Honeybees use optic flow to measure the distance of a food source.Naturwissenschaft,82, 38–40.
Etienne, A. S., Berlie, J., Georgakopoulos, J., &Maurer, R. (1998). Role of dead reckoning in navigation. In S. Healy (Ed.),Spatial representation in animals (pp. 54–68). Oxford: Oxford University Press.
Etienne, A. S., Joris-Lambert, S., Dahn-Hurni, C., &Reverdin, B. (1995). Optimizing visual landmarks: Two and three dimensional minimal landscapes.Animal Behaviour,49, 165–179.
Etienne, A. S., Joris-Lambert, S., Maurer, R., Reverdin, B., &Sitbon, S. (1995). Optimizing distal landmarks: Horizontal versus vertical structures and relation to background.Behavioural Brain Research,68, 103–116.
Etienne, A., Teroni, E., Hurni, C., &Portenier, V. (1990). The effect of a single light cue on homing behaviour of the golden hamster.Animal Behaviour,39, 17–41.
Frier, H. J., Edwards, E., Smith, C., Neal, S., &Collett, T. S. (1996). Magnetic compass cues and visual pattern learning in honeybees.Journal of Experimental Biology,199, 1353–1361.
Gallistel, C. R. (1990).The organization of learning. Cambridge, MA: MIT Press.
Giurfa, M., &Vorobyev, M. (1998). The angular range of achromatic target detection by honeybees.Journal of Comparative Physiology A,183, 101–110.
Giurfa, M., Vorobyev, M., Brandt, R., Posner B., &Menzel, R. (1997). Discrimination of coloured stimuli by honeybees: Alternative use of achromatic and chromatic signals.Journal of Comparative Physiology A,180, 235–243.
Giurfa, M., Vorobyev, M., Kevan, P., &Menzel, R. (1996). Detection of coloured stimuli by honeybees: Minimum visual angles and receptor specific contrasts.Journal of Comparative Physiology A,178, 699–709.
Gould, J. L. (1986). The locale map of honey bees: Do insects have cognitive maps?Science,232, 861–863.
Gould, J. L. (1987). Landmark learning by honey bees.Animal Behaviour,35, 26–34.
Healy S. (Ed.) (1998).Spatial representation in animals. Oxford: Oxford University Press.
Hempel de Ibarra, N.,Brandt, R.,Giurfa, M., &Vorobyev, M. (1998, August).Can honeybees detect white flowers? Poster presented at the Fifth International Congress of Neuroethology, San Diego, CA.
Hermer, L., &Spelke, E. (1996). Modularity and development: The case of spatial orientation.Cognition,61, 195–232.
Isnec, M. R., Couvillon, P. A., &Bitterman, M. E. (1997). Shortterm spatial memory in honeybees.Animal Learning & Behavior,25, 165–170.
Judd, S. P. D., &Collett, T. S. (1998). Multiple stored views and landmark guidance in ants.Nature,392, 710–714.
Labhart, T. (1988). Polarization-opponent interneurons in the insect visual system.Nature,331, 435–437.
Lehrer, M. (1993). Why do bees turn back and look?Journal of Comparative Physiology A,172, 549–563.
Lehrer, M. (1994). Spatial vision in the honeybee: The use of different cues in different tasks.Vision Research,34, 2363–2385.
Lehrer, M. (1996). Small-scale navigation in the honeybee: Active acquisition of visual information about the goal.Journal of Experimental Biology,199, 253–261.
Lehrer, M., &Collett, T. S. (1994). Approaching and departing bees learn different cues to the distance of a landmark.Journal of Comparative Physiology A,175, 171–177.
Lehrer, M., Srinivasan, M. V., Zhang, S. W., &Horridge, G. A. (1988). Motion cues provide the bee’s visual world with a third dimension.Nature,332, 356–357.
Meck, W. H. (1983). Selective adjustment of the speed of internal clock and memory processes.Journal of Experimental Psychology: Animal Behavior Processes,9, 171–201.
Menzel, R., Geiger, K., Jeorges, J., Müller, U., &Chittka, L. (1998). Bees travel novel homeward routes by integrating separately acquired vector memories.Animal Behaviour,55, 139–152.
Müller, M., &Wehner, R. (1988). Path integration in desert ants,Cataglyphis fortis.Proceedings of the National Academy of Sciences,85, 5287–5290.
Platt, J. R., &Davis, E. R. (1983). Bisection of temporal intervals by pigeons.Journal of Experimental Psychology: Animal Behavior Processes,9, 160–170.
Rakitin, B. C., Gibbon, J., Penney, T., Malapani, C., Hinton, S. C., &Meck, W. H. (1998). Scalar expectancy theory and peak-interval timing in humans.Journal of Experimental Psychology: Animal Behavior Processes,24, 15–33.
Roberts, W. A. (1998).Principles of animal cognition. Boston: McGraw-Hill.
Ronacher, B.,Gallizzi, K.,Wohlgemuth S., &Wehner, R. (in press). Lateral optic flow does not influence distance estimation in the desert antCataglyphis fortis.Journal of Experimental Biology.
Ronacher, B., &Wehner, R. (1995). Desert antsCataglyphis fortis use self-induced optic flow to measure distances travelled.Journal of Comparative Physiology A,177, 21–27.
Schmidt, R. F. (Ed.) (1981).Fundamentals of sensory physiology. New York: Springer-Verlag.
Schöne, H. (1996). Optokinetic speed control and estimation of travel distance in walking honeybees.Journal of Comparative Physiology A,179, 587–592.
Seeley, T. D. (1985).Honeybee ecology: A study of adaptation in social life. Princeton, NJ: Princeton University Press.
Seeley, T. D. (1995).The wisdom of the hive: The social physiology of honey bee colonies. Cambridge, MA: Harvard University Press.
Shepard, R. N. (1987). Toward a universal law of generalization for psychological science.Science,237, 1317–1323.
Shettleworth, S. J. (1998).Cognition, evolution, and behavior. New York: Oxford University Press.
Srinivasan, M. V., Lehrer, M., Zhang, S. W., &Horridge, G. A. (1989). How honeybees measure their distance from objects of unknown size.Journal of Comparative Physiology A,165, 605–613.
Srinivasan, M. V., Zhang, S. W., Berry, J., Cheng, K., &Zhu, H. (1999). Honeybee navigation: Linear perception of short distances travelled.Journal of Comparative Physiology A,185, 239–245.
Srinivasan, M. V., Zhang, S. W., &Bidwell, N. J. (1997). Visually mediated odometry in honeybees.Journal of Experimental Biology,200, 2513–2522.
Srinivasan, M. V., Zhang, S. W., &Lehrer, M. (1998). Honeybee navigation: Odometry with monocular input.Animal Behaviour,56, 1245–1259.
Srinivasan, M. V., Zhang, S. W., Lehrer, M., &Collett, T. S. (1996). Honeybee navigation en route to the goal: Visual flight control and odometry.Journal of Experimental Biology,199, 155–162.
Suzuki, S., Augerinos, G., &Black, A. (1980). Stimulus control of spatial behavior on the eight-arm maze in rats.Learning & Motivation,11, 1–18.
Tinbergen, N. (1972).The animal in its world. Cambridge, MA: Harvard University Press.
Vauclair, J. (1996).Animal cognition: An introduction to modern comparative psychology. Cambridge, MA: Harvard University Press.
von Frisch, K. (1953).The dancing bees (D. Ilse, Trans.). San Diego, CA: Harcourt Brace Jovanovich.
Wearden, J. H. (1991). Human performance on an analogue of an interval bisection task.Quarterly Journal of Experimental Psychology,43B, 59–81.
Wehner, R. (1994). The polarization-vision project: Championing organismic biology.Fortschritte der Zoologie,39, 103–143.
Wehner, R., Bleuler, S., Nievergelt, C., &Shah, D. (1990). Bees navigate by using vectors and routes rather than maps.Naturwissenschaften,77, 479–482.
Wehner, R.,Lehrer, M., &Harvey, P. (Eds.) (1996). Navigation.Journal of Experimental Biology,199, 1–261.
Wehner, R., &Menzel, R. (1990). Do insects have cognitive maps?Annual Review of Neurosciences,13, 403–414.
Wehner, R., Michel, B., &Antonsen, P. (1996). Visual navigation in insects: Coupling of egocentric and geocentric information.Journal of Experimental Biology,199, 129–140.
Wehner, R., &Müller, M. (1993). How do ants acquire their celestial ephemeris function?Naturwissenschaften,80, 331–333.
Wehner R., &Wehner, S. (1990). Insect navigation: Use of maps or Ariadne’s thread?Ethology, Ecology, & Evolution,2, 27–48.
Zeil, J. (1993a). Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera): I. Description of flight.Journal of Comparative Physiology A,172, 189–205.
Zeil, J. (1993b). Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera): II. Similarities between orientation and return flights and the use of motion parallax.Journal of Comparative Physiology A,172, 207–222.
Author information
Authors and Affiliations
Corresponding author
Additional information
This research was supported by grants from the Australian Research Council and from Macquarie University. The author thanks Mike Brown, Thomas Collett, Martin Giurfa, Sara Shettleworth, and Mandyam Srinivasan for comments.
Rights and permissions
About this article
Cite this article
Cheng, K. How honeybees find a place: Lessons from a simple mind. Animal Learning & Behavior 28, 1–15 (2000). https://doi.org/10.3758/BF03199768
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/BF03199768