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The memory structure of navigation in honeybees

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Abstract

The analytical approach to navigation studies aims to identify elementary sensory motor processes that guide an animal to a remote site. This approach will be used here to characterize components of navigation in a flying insect, the honeybee. However, navigation studies need to go beyond an analysis of behavioral routines to come up with a synthesis. We will defend the concept of an active memory structure guiding navigation in bees that is best described as a mental or cognitive map. In our opinion, spatial/temporal relations of landmarks are stored in a mental map in such a way that behavioral routines such as expectation and planning, as indicated by shortcutting, are possible. We view the mental map of animals including the honeybee as an “action memory of spatial relations” rather than as a sensory representation as we humans experience it by introspection. Two components characterize the mental map, the relational representation of landmarks and the meaning of locations to the animal. As yet, there is little data to suggest that bees assign meaning to the experienced locations. To explore this possibility, further studies will be needed, whereby honeybees provide a unique model to address this question.

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References

  • Barnett SA (1958) Exploratory behaviour. Brit J Psychol 49(4):289–310

    Article  CAS  PubMed  Google Scholar 

  • Becker L (1958) Untersuchungen über das Heimfindevermögen der Bienen. Z vergl Physiol 41:1–25

    Google Scholar 

  • Biegler R (2000) Possible uses of path integration in animal navigation. Anim Learn Behav 28(3):257–277

    Article  Google Scholar 

  • Blodgett HC (1929) The effect of the introduction of reward upon the maze performance of rats. Univ Cal Publ Psychol 4:113–134

    Google Scholar 

  • Capaldi EA, Dyer FC (1999) The role of orientation flights on homing performance in honeybees. J Exp Biol 202:1655–1666

    CAS  PubMed  Google Scholar 

  • Capaldi EA, Smith AD, Osborne JL, Fahrbach SE, Farris SM, Reynolds DR, Edwards AS, Martin A, Robinson GE, Poppy GM, Riley JR (2000) Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403:537–540

    Article  CAS  PubMed  Google Scholar 

  • Cheeseman JF, Millar CD, Greggers U, Lehmann K, Pawley MD, Gallistel CR, Warman GR, Menzel R (2014a) Way-finding in displaced clock-shifted bees proves bees use a cognitive map. Proc Natl Acad Sci USA 111(24):8949–8954

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheeseman JF, Millar CD, Greggers U, Lehmann K, Pawley MD, Gallistel CR, Warman GR, Menzel R (2014b) Reply to Cheung et al.: The cognitive map hypothesis remains the best interpretation of the data in honeybee navigation. PNAS 2014; published ahead of print October 2, 2014. doi:10.1073/pnas.1415738111

  • Cheung A, Collett M, Collett TS, Dewar A, Dyer F, Graham P, Mangan M, Narendra A, Philippides A, Stürzl W, Webb B, Wystrach A, Zeil J (2014) Still no convincing evidence for cognitive map use by honeybees. PNAS 2014; published ahead of print October 2, 2014. doi:10.1073/pnas.1413581111

  • Chittka L, Geiger K (1995) Can honeybees count landmarks? Anim Behav 49:159–164

    Article  Google Scholar 

  • Chittka L, Geiger K, Kunze J (1995) The influences of landmarks on distance estimation of honey bees. Anim Behav 50:23–31

    Article  Google Scholar 

  • Clark A (1998) Being there: putting brain, body, and world together again. MIT Press, Boston

    Google Scholar 

  • Collett TS, Kelber A (1988) The retrieval of visuo-spatial memories by honeybees. J Comp Physiol A 163(1):145–150

    Article  CAS  PubMed  Google Scholar 

  • Cruse H, Wehner R (2011) No need for a cognitive map: decentralized memory for insect navigation. PLoS Comput Biol 7(3):e1002009

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Marco RJ, Menzel R (2005) Encoding spatial information in the waggle dance. J Exp Biol 208:3885–3894

    Article  PubMed  Google Scholar 

  • Degen J, Kirbach A, Reiter L, Lehmann K, Norton P, Storms M, Koblofsky M, Jones S, Georgieva PB, Nguyen H, Chamkhi H, Greggers U, Menzel R (2015) Honeybees apply effective exploration strategies during orientation flights. Anim Behav

  • Dyer FC, Gould JL (1981) Honey bee orientation: a backup system for cloudy days. Science 214:1041–1042

    Article  CAS  PubMed  Google Scholar 

  • Engel AK, Maye A, Kurthen M, Konig P (2013) Where’s the action? The pragmatic turn in cognitive science. Trends Cogn Sci 17(5):202–209

    Article  PubMed  Google Scholar 

  • Fischer J, Muller T, Spatz AK, Greggers U, Grunewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One 9(3):e91364

    Article  PubMed Central  PubMed  Google Scholar 

  • Gallistel CR (1990) The organization of learning. Cambridge, Mass. MIT Press, London

    Google Scholar 

  • Gould JL (1986) Landmark learning by honey bees. Anim Behav 35:26–34

    Article  Google Scholar 

  • Greggers U, Mauelshagen J (1997) Matching behavior of honeybees in a multiple-choice situation: the differential effect of environmental stimuli on the choice process. Anim Learn Behav 25(4):458–472

    Article  Google Scholar 

  • Gruter C, Farina WM (2009) The honeybee waggle dance: can we follow the steps? Trends Ecol Evol 24(5):242–247

    Article  PubMed  Google Scholar 

  • Gruter C, Leadbeater E (2014) Insights from insects about adaptive social information use. Trends Ecol Evol 29(3):177–184

    Article  PubMed  Google Scholar 

  • Hartmann G, Wehner R (1995) The ant’s path integration system: a neural architecture. Biol Cybern 73:483–497

    Google Scholar 

  • Hommel B, Elsner B (2009) Acquisition, representation, and control of action. In: Morsella E (ed) Oxford handbook of human action. Oxford University Press, Oxford, pp 371–398

    Google Scholar 

  • Jacobs LF, Schenk F (2003) Unpacking the cognitive map: the parallel map theory of hippocampal function. Psychol Rev 110:285–315

    Article  PubMed  Google Scholar 

  • Jacobs LF, Menzel R (2014) Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab. Mov Ecol 2(3):1–22

    CAS  Google Scholar 

  • Kemfort JR, Towne WF (2013) Honeybees can learn the relationship between the solar ephemeris and a newly experienced landscape: a confirmation. J Exp Biol 216(Pt 20):3767–3771

    Article  PubMed  Google Scholar 

  • Kramer G (1952) Experiments on bird orientation. Ibis 94:265–285

    Article  Google Scholar 

  • Lehrer M (1993) Why do bees turn back and look? J Comp Physiol [A] 172:549–563

    Article  Google Scholar 

  • Lehrer M (1997) Honeybees' visual spatial orientation at the feeding site. In: Lehrer M (ed) Detection and Comunication in Arthropods. Birkhäuser, Basel, pp 115–44

  • Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z vergl Physiol 34:299–345

    Article  Google Scholar 

  • Locke NM (1936) A preliminary study of the social drive in the white rat. J Psychol 1:255–260

    Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7(8):663–678

    Article  CAS  PubMed  Google Scholar 

  • Menzel R (2009) Serial position learning in honeybees. PLoS One 4:e4694–e4701

    Article  PubMed Central  PubMed  Google Scholar 

  • Menzel R (2013) The cognitive structure of visual navigation in honeybees. In: Werner JS, Chalupa LM (eds) The new visual neuroscience. MIT Press, Cambridge, pp 1179–1189

    Google Scholar 

  • Menzel R, Greggers U (2013) Guidance by odors in honeybee navigation. J Comp Physiol A 199(10):867–873

    Article  CAS  Google Scholar 

  • Menzel R, Geiger K, Müller U, Joerges J, Chittka L (1998) Bees travel novel homeward routes by integrating separately acquired vector memories. Anim Behav 55:139–152

    Article  PubMed  Google Scholar 

  • Menzel R, Brandt R, Gumbert A, Komischke B, Kunze J (2000) Two spatial memories for honeybee navigation. Proc R Soc Lond B Biol Sci 267(1447):961–968

    Article  CAS  Google Scholar 

  • Menzel R, Greggers U, Smith A, Berger S, Brandt R, Brunke S, Bundrock G, Hulse S, Plumpe T, Schaupp F, Schuttler 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(8):3040–3045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Menzel R, De Marco RJ, Greggers U (2006) Spatial memory, navigation and dance behaviour in Apis mellifera. J Comp Physiol A 192(9):889–903

    Article  Google Scholar 

  • Menzel R, Fuchs J, Nadler L, Weiss B, Kumbischinski N, Adebiyi D, Hartfil S, Greggers U (2010) Dominance of the odometer over serial landmark learning in honeybee navigation. Naturwiss 97(8):763–767

    Article  CAS  PubMed  Google Scholar 

  • Menzel R, Kirbach A, Haass W-D, Fischer B, Fuchs J, Koblofsky M, Lehmann K, Reiter L, Meyer H, Nguyen H, Jones S, Norton P, Greggers U (2011) A common frame of reference for learned and communicated vectors in honeybee navigation. Curr Biol 21:645–650

    Article  CAS  PubMed  Google Scholar 

  • Menzel R, Lehmann K, Manz G, Fuchs J, Kobolofsky MGU (2012) Vector integration and novel shortcutting in honeybee navigation. Apidologie 43:229–243. doi:10.1007/s13592-012-0127-z

    Article  Google Scholar 

  • Montgomery KC (1954) The role of the exploratory drive in learning. J Comp Physiol Psychol 47(1):60–64

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Wehner R (1988) Path integration in desert ants, Cataglyphis fortis. Proc Natl Acad Sci USA 85:5287–5290

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Keefe J (1991) An allocentric spatial model for the hippocampal cognitive map. Hippocampus 1:230–235

    Article  PubMed  Google Scholar 

  • O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428

    Article  PubMed  Google Scholar 

  • O’Keefe J, Nadel J (1978) The hippocampus as a cognitive map. Oxford University Press, New York

    Google Scholar 

  • Opfinger E (1931) Über die Orientierung der Biene an der Futterquelle. Z vergl Physiol 15:432–487

    Article  Google Scholar 

  • Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybees recruited by the waggle dance. Nature 435(7039):205–207

    Article  CAS  PubMed  Google Scholar 

  • Seeley TD (2011) Honeybee democracy. Princeton University Press, Princeton

    Google Scholar 

  • Small WS (1899) Notes on the psychic development of the young white rat. Am J Psychol 11:80–100

    Article  Google Scholar 

  • Tan K, Hu Z, Chen W, Wang Z, Wang Y, Nieh JC (2013) Fearful foragers: honey bees tune colony and individual foraging to multi-predator presence and food quality. PLoS One 8(9):e75841

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thorpe WH (1963) Learning and instinct in animals. Methuen, London

    Google Scholar 

  • Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208

    Article  CAS  PubMed  Google Scholar 

  • Tolman EC (1932) Purposive behavior in animals and men. Century, New York

    Google Scholar 

  • Touretzky DS, Redish AD (1995) Landmark arrays and the Hippocampal cognitive map. In: Proceedings of the 1995 Swedish conference on connectionism (submitted)

  • Towne WF (2008) Honeybees can learn the relationship between the solar ephemeris and a newly-experienced landscape. J Exp Biol 211(Pt 23):3737–3743

    Article  PubMed  Google Scholar 

  • Towne WF, Moscrip H (2008) The connection between landscapes and the solar ephemeris in honeybees. J Exp Biol 211(Pt 23):3729–3736

    Article  PubMed  Google Scholar 

  • Vollbehr J (1975) Zur Orientierung junger Honigbienen bei ihrem 1. Orientierungsflug. Zool Jb Physiol 79:33–69

    Google Scholar 

  • von Frisch K (1946) Die tänze der bienen. Österr Zool Zeit 1:1–48

    Google Scholar 

  • von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge

    Google Scholar 

  • von Frisch K, Lindauer M (1954) Himmel und erde in konkurrenz bei der orientierung der bienen. Naturwissenschaften 41:245–253

    Article  Google Scholar 

  • Wehner R, Menzel R (1990) Do insects have cognitive maps? Annu Rev Neurosci 13:403–414

    Article  CAS  PubMed  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • Zeil J (1993) Orientation flights of solitary wasps (Cerceris; Specidae; Hymenoptera) I. Description of flight. J Comp Physiol [A] 172:189–205

    Article  Google Scholar 

  • 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(14):5250–5255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We are most grateful to the large number of students who helped us with the field experiments over the years. We wish to thank in particular Konstantin Lehmann, Jacqueline Degen, Andreas Kirbach and Tim Landgraf for their most valuable contributions. We are also grateful to J. R. Riley, A. M. Reynolds and A. D. Smith for introducing us to the harmonic radar tracking of bees. Work with the radar tracking technique was supported by grants from the Deutsche Forschungsgemeinschaft (DFG Me 365/25-1 und 25-2) and the Deutscher Akademischer Austauschdienst. RM received in addition grants from the Dr. Klaus Tschira Stiftung and from the Gemeinnützige Hertie Stiftung. UG was supported by the Olin Stiftung.

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  1. Freie Universität, Berlin, Germany

    Randolf Menzel & Uwe Greggers

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  1. Randolf Menzel
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  2. Uwe Greggers
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Correspondence to Randolf Menzel.

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Menzel, R., Greggers, U. The memory structure of navigation in honeybees. J Comp Physiol A 201, 547–561 (2015). https://doi.org/10.1007/s00359-015-0987-6

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