Skip to main content
SpringerLink
Log in

Maze Navigation and Route Memorization by Worker Bumblebees (Bombus impatiens (Cresson) (Hymenoptera: Apidae)

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

Bumblebees move about their environments by flying and by walking. Most experimental studies have addressed navigation during foraging flights, but we presented our experimental bees with the challenge of learning to navigate while walking as they must do in nature within topographically complex spaces containing their nests. We trained bumblebee workers to navigate complex, nine-channel, mazes in the absence of specific visual, chemical or textural cues. They successfully navigated through complex multi-turn mazes (stereotypical “rat mazes”) with several dead-ends by memorizing the entire sequence of appropriate turns, and their choice of correct first turn on entering the maze. Thus, their observed proficiencies indicated that the individual bumblebees had each memorized the maze by learning motor sequences which were not linked to visual, chemical or textural stimuli, and that their memories were triggered by contextual cues associated with the bees’ positions in a sequence. Our findings have implications on natural ambulatory activities inside and outside the colony, and even in practical use as vectors of biological control agents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson JR (2000) Learning and memory an integrated approach (second edition). Wiley, Carnegie Mellon University

    Google Scholar 

  • Baerends GP (1941) Fortpflanzungsverhalten und Orientierung der grabwespe Ammophila campestris Jur. Zietschrifte für Entomologie 84:81–275

    Google Scholar 

  • Bernstein S, Bernstein RA (1969) Relationship between foraging efficiency and the size of the head and component. Brain Res 16:85–104

    Article  CAS  PubMed  Google Scholar 

  • Bicker G, Spatz HC (1976) Maze-learning ability of Drosophila melanogaster. Nature 260:371

    Article  Google Scholar 

  • Cameron SA (1985) Brood care by male bumble bees. Proc Natl Acad Sci U S A 82:6371–6373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cameron SA, Whitfield JB (1996) Use of walking trails by bees. Nature 379:125

    Article  CAS  Google Scholar 

  • Cartron L, Darmaillacq SA, Jozet-Alves C, Shashar N, Dickel L (2012) Cuttlefish rely on both polarized light and landmarks for orientation. Anim Cogn 15: 591–596

  • Chameron S, Schatz B, Pastergue-Ruiz I, Beugnon G, Collett TS (1998) The learning of a sequence of visual patterns by the ant Cataglyphis cursor. Proc R Soc Lond B Biol Sci 265:2309–2313

    Article  Google Scholar 

  • Chittka L (1998) Sensorimotor learning in bumblebees: long-term retention and reversal training. J Exp Biol 201:515–524

    Google Scholar 

  • Chittka L, Thomson JD (1996) The ecology of bumble bees in T- mazes. In: Gőttingen Neurobiology Report. Elsner N, Schnitzler H. (eds). Thieme, Stuttgart, p 130

  • Chittka L, Thomson JD (1997) Sensori-motor learning and its relevance for task specialization in bumble bees. Behav Ecol Sociobiol 41:385–398

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Collett TS (1992) Landmark learning and guidance in insects. Philos Trans R Soc Lond Ser B Biol Sci 337:295–303

    Article  Google Scholar 

  • Collett TS, Baron J (1995) Learnt sensori-motor mappings in honeybees: interpolation and its possible relevance to navigation. J Com Physiol Series A 177:287–298

    Google Scholar 

  • Collett TS, Zeil J (1998) Place and landmarks: An arthropod perspective. In: Spatial Representation in Animals (ed. S. Healy), pp. 18–53. Oxford University Press, Oxford

  • Collett TS, Dillmann E, Giger A, Wehner R (1992) Visual landmarks and route following in desert ants. J Comp Physiol, Series A 170:435–442

    Google Scholar 

  • Collett TS, Fry SN, Wehner R (1993) Sequence learning by honeybees. J Com Physiol Series A 172:693–706

    Google Scholar 

  • Corbet SA, Kerslake CJC, Brown D, Morland NE (1984) Can bees select nectar-rich flowers in a patch? J Apic Res 23:234–247

    Google Scholar 

  • Dale RHI (1988) Spatial memory in pigeons on a four-arm radial maze. Can J Psychol 42:78–83

    Article  CAS  PubMed  Google Scholar 

  • Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod Plant Interact 1:45–55

    Article  Google Scholar 

  • Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Com Physio, Series A 194:617–627

    Article  Google Scholar 

  • Free JB (1987) Pheromones of social bees. Chapman and Hall, London, UK

    Google Scholar 

  • Free JB, Butler CG (1959) Bumblebees. Collins, London

    Google Scholar 

  • Gallistel CR (1990) The cognitive map. In: Gallistel CR (ed) The organisation of learning. MIT Press, Cambridge, pp 103–172

    Google Scholar 

  • Goetsch W (1957) The Ants. The University of Michigan Press

  • Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Goulson D, Stout JC, Langley J, Hughes WHO (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911

    Article  CAS  Google Scholar 

  • Han P, Niu C, Lei C, Cui J, Desneux N (2010) Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee. Apis mellifera L Ecotoxicol 19:1612–1619

    Article  CAS  Google Scholar 

  • Hay DA (1975) Strain differences in maze-learning ability of Drosophila melanogaster. Nature 257:44–46

    Article  CAS  PubMed  Google Scholar 

  • Healy S (1998) Spatial Representation in Animals. Oxford University Press, Oxford

    Google Scholar 

  • Heinrich B (1976) Foraging specialisations of individual bumblebees. Ecol Monogr 46:105–128

    Article  Google Scholar 

  • Honzik CH (1936) The sensory basis of maze learning in rats. Com Psychol Monog 13:113

    Google Scholar 

  • Janzen DH (1971) Euglossine bees as long distance pollinators of tropical plants. Science 171:203–205

    Article  CAS  PubMed  Google Scholar 

  • Keasar T, Motro U, Shur Y, Shmida A (1996) Overnight memory retention of foraging skills by bumblebees is imperfect. Anim Behav 52:95–104

    Article  Google Scholar 

  • Kevan PG (1979) Floral colors in the high arctic with reference to insect–flower relations and pollination. Can J Bot 50:2289–2316

    Article  Google Scholar 

  • Kevan PG (1979) The spectral efficiency of phototaxis for some high Arctic Diptera. Arct Alp Res 11:349–352

    Article  Google Scholar 

  • Kevan PG, Lane MA (1985) Flower petal microtexture is a tactile cue for bees. Proc Natl Acad Sci U S A 80:4750–4752

    Article  Google Scholar 

  • Kevan PG, Kapongo JP, Al-Mazra’awi M, Shipp L (2008) Honey bees, bumble bees, and biocontrol. In: Bee Pollination in Agricultural Ecosystems (eds James, RR, Pitts-Singer TL). Oxford University Press. Pp. 65 – 79.

  • Kevan PG, Shipp L, Thomas VG (2014) Using pollinators for crop protection. Int Innov 125:9–11

    Google Scholar 

  • Lehrer M, Horridge GA, Zhang SW, Gadagkar R (1995) Shape vision in bees: Innate preference for flower-like patterns. Philos Trans R Soc Lond B 347:123–137

    Article  Google Scholar 

  • Lihoreau M, Raine NE, Reynolds AM, Stelzer RJ, Lim KS, Smith AD, Osborne JL, Chittka L (2012) Radar tracking and motion-sensitive cameras on flowers reveal the development of pollinator multi-destination routes over large spatial scales. PLoS Biol 10(9), e1001392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin H (1965) Leistungen des topochemischen Sinnes bei der Honigbiene. Zeitsehrift fiir vergleichende Physiologie 50:254–292

    Google Scholar 

  • McConnell JV (1966) The Worm Runner’s Digest. The Sciences 6(7): 19–23

  • Menzel R (1981) Achromatic vision in the honeybee at low light intensities. J Comp Physiol Series A 141:389–393

    Article  Google Scholar 

  • Menzel R (1990) Learning, memory and ‘cognition’ in honey bees. In: Kesner RP, Olten DS (eds) Neurobiology of Comparative Cognition. Erlbaum Inc., Hillsdale, NJ, pp 237–292

    Google Scholar 

  • Mirwan HB, Kevan PG (2014) Problem solving by worker bumblebees Bombus impatiens (Hymenoptera: Apoidea). Anim Cogn. doi:10.1007/s10071-014-0737-0

    PubMed  Google Scholar 

  • Muller M, Wehner B (1988) Path integration in desert ants, Cataglyphis fortis. Neurobiology 85:5287–5290

    CAS  Google Scholar 

  • Munn NL (1950) The role of sensory processes in maze behavior. In: Handbook of Psychological Research on the Rat, (Munn NL). Houghton Mifflin, Boston, pp 181–225

    Google Scholar 

  • Ohashi K, Thomson JD (2012) Trapline foraging by bumble bees: VI. Behavioral Alter Under Speed-Accuracy Trade-offs Behav Ecol 24:182–189

    Google Scholar 

  • Olton DS (1977) Spatial memory. Sci Am 236(6):82–98

    Article  CAS  PubMed  Google Scholar 

  • Pick CG, Yanai J (1983) Eight arm maze for mice. Int J Neurosci 21:63–66

    Article  CAS  PubMed  Google Scholar 

  • Platt SA, Holliday M, Drudge OW (1980) Discrimination learning of an instrumental response in individual Drosophila melanogaster. J Exp Psychol Anim Behav Process 6:301–311

    Article  CAS  PubMed  Google Scholar 

  • Plowright CMS, Simonds VM, Butler MA (2006) How bumblebees first find flowers: Habituation of visual pattern preferences, spontaneous recovery, and dishabituation. Learn Motiv 37:66–78

    Article  Google Scholar 

  • Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 71:708–712

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumblebees. Proc Royal Soci London Series B-Biolog Sci 275:803–808

    Article  Google Scholar 

  • Reynolds AM, Lihoreau M, Chittka L (2013) A simple iterative model accurately captures complex trapline formation by bumblebees accross spatial scales and flower arrangements. PLoS Comput Biol 9, e1002938

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ritter, FE & Schooler LJ (2002) The learning curve. In International encyclopedia ofthe social and behavioral sciences. 8602–8605. Amsterdam: Pergamon. http://www.iesbs.com/

  • Rosengren R (1971) Route fidelity, visual memory and recruitment behaviour in foraging wood ants of the genus Formica (Hymenoptera, Formicidae). Acta Zool Fenn 133:1–106

    Google Scholar 

  • 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 Interact 1:119–127

    Article  Google Scholar 

  • SAS (Statistical Analaysis Software) (2014) www.sas.com/en_us/software/analytics/stat.html (accessed 11 September, 2014)

  • Schneirla TC (1929) Learning and orientation in ants. Comparative Psychology Monographs 6:1–143

    Google Scholar 

  • Schneirla TC (1941) Social organization in insects, as related to individual function. Psychol Rev 48:465–486

    Article  Google Scholar 

  • Séguin FR, Plowright CMS (2008) Assessment of pattern preferences by flower-naïve bumblebees. Apidologie 39:215–224

    Article  Google Scholar 

  • Sladen FWL (1912) The humble-bee its life history and how to domesticate it. With description of all British species of Bombus and Psithyrus. Macmillan & Co., Ltd

  • Tierney AJ; Andrews K (2013) Spatial behavior in male and female crayfish (Orconectes rusticus): learning strategies and memory duration. Anim Cogn 16:23–34

  • Thomson JD, Slatkin M, Thomson BA (1997) Trapline foraging by bumblebees definition and detection from sequence data. Behav Ecol 8:199–210

    Article  Google Scholar 

  • Thorpe WH (1950) A note on detour experiment with Ammophila pubescens Curt. (Hymenoptera; Sphecidae). Behaviour 13:257–263

    Article  Google Scholar 

  • Tully T (1984) Drosophila learning: Behavior and biochemistry. Behav Genet 14:527–557

    Article  CAS  PubMed  Google Scholar 

  • Vygotsky LS (1987) Thinking and speech. In L. S. Vygotsky, Collected works (1: pp. 39–285) (R. Rieber & A. Carton, Eds; N. Minick, Trans). New York: Plenum. (Original works published in 1934, 1960).

  • Wehner R (1992) Arthropods. In: Papi F (ed) Animal Homing. Chapman & Hall, London, pp 45–144

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140

    PubMed  Google Scholar 

  • Weiss K (1953) Versuche mit Bienen und Wespen in farbingen Labyrinthen. Zeitschifte für Tierpsychologie 10:29–44

    Article  Google Scholar 

  • Wilms J, Eltz T (2008) Foraging scent marks of bumblebees: footprint cues rather than pheromone signals. Naturwissenschaften 95:149–153

    Article  CAS  PubMed  Google Scholar 

  • Wilson EO, Hölldobler B (1990) The ants. Springer, Berlin Heidelberg

    Google Scholar 

  • Zhang SW, Bartsch K, Srinivasan MV (1996) Maze learning by honeybees. Neurobiol Learn Mem 66:267–282

    Article  CAS  PubMed  Google Scholar 

  • Zhang SW, Lehrer M, Srinivasan MV (1998) Stimulus- conditioned sequence learning in honeybees. In: Proceedings of the 26th Goettingen Neurobiology Conference 1998 (eds Elsner N and Wehner R), 2: 519. Stuttgart: Thieme

  • Zhang SW, Lehrer M, Srinivasan MV (1999) Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol Learn Mem 72:180–201

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Mizutani A, Srinivasan MV (2000) Maze navigation by honeybees: learning path regularity. Learn Mem 7:363–374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Ministry of Higher Education, Libya, Canadian Bureau for International Education, Ottawa, Canada, and the Canadian Pollination Initiative (NSERC-CANPOLIN for which this is contribution No. 128) for funding. We thank Dr. Sarah Bates (NSERC-CANPOLIN, University of Guelph) for her help in preparing this paper. BioBest Canada, Leamington, Ontario kindly provided the colonies of Bombus impatiens for our study.

Author information

Authors and Affiliations

  1. School of Environmental Sciences and The Canadian Pollination Initiative, University of Guelph, Guelph, ON, N1G 2 W1, Canada

    Hamida B. Mirwan & Peter G. Kevan

Authors
  1. Hamida B. Mirwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter G. Kevan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter G. Kevan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mirwan, H.B., Kevan, P.G. Maze Navigation and Route Memorization by Worker Bumblebees (Bombus impatiens (Cresson) (Hymenoptera: Apidae). J Insect Behav 28, 345–357 (2015). https://doi.org/10.1007/s10905-015-9507-3

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-015-9507-3

Keywords

Search

Navigation