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A new protocol for measuring spatial learning and memory in the honey bee Apis mellifera: effects of behavioural state and cGMP

  • N. Tsvetkov
  • B. Madani
  • L. Krimus
  • S. E. MacDonald
  • A. Zayed
Research Article

Abstract

The honey bee Apis mellifera is a model organism for studying learning and memory in insects. Although much work has been done to study olfactory learning using the proboscis extension reflex paradigm, we currently lack a high throughput method to study spatial learning and memory under controlled conditions. Here we outline a new paradigm to study spatial learning and memory in honey bees based on a food search task adopted from the vertebrate literature. After establishing that honey bees are able to learn and recall the location of artificial flowers inside the testing arena, we used the procedure to compare the performance of young nurse bees, who stay in the colony and nurse the brood, and old forager bees who forage outside. We also compared the spatial learning and memory of age-staged bees that were experimentally treated with cyclic guanosine monophosphate (cGMP), which causes precocious foraging, and cyclic adenosine monophosphate (cAMP), which does not alter behavioural state. Although foragers and nurses from typical colonies had similar learning curves, we found that foragers were significantly more accurate when recalling the location of previously rewarding artificial flowers inside the testing arena. This effect was also observed when comparing age-staged bees that have been chronically exposed to cGMP vs. those chronically exposed to cAMP. The Food Search Box paradigm is a simple and effective way to study spatial learning and memory in honey bees.

Keywords

Spatial learning and memory Honey bee Behavioural state Apis mellifera 

Notes

Acknowledgements

This study was funded by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada and an Early Researcher Award from the Ontario Ministry of Research and Innovation to AZ. NT was supported by a Graduate Scholarship from the Province of Ontario and a York University Graduate Scholarship.

References

  1. Ben-Shahar Y, Dudek NL, Robinson GE (2004) Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J Exp Biol 207:3281–3288CrossRefPubMedGoogle Scholar
  2. Ben-Shahar Y, Robichon A, Sokolowski M, Robinson G (2002) Influence of gene action across different time scales on behavior. Science 296:741–744CrossRefPubMedGoogle Scholar
  3. Chauvin C, Thierry B (2005) Tonkean macaques orient their food search from olfactory cues conveyed by conspecifics. Ethology 111:301–310CrossRefGoogle Scholar
  4. Clayton N, Krebs J (1994) Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 174:371–379Google Scholar
  5. Durst C, Eichmüller S, Menzel R (1994) Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neural Biol 62:259–263CrossRefPubMedGoogle Scholar
  6. Dyer FC, Berry NA, Richard AS (1993) Honey bee spatial memory: use of route-based memories after displacement. Anim Behav 45:1028–1030CrossRefGoogle Scholar
  7. 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
  8. Harpur B et al (2015) Assessing patterns of admixture and ancestry in Canadian honey bees. Insectes Soc 62:479–489CrossRefGoogle Scholar
  9. Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Mol Ecol 21:4414–4421CrossRefPubMedGoogle Scholar
  10. Harpur BA, Minaei S, Kent CF, Zayed A (2013) Admixture increases diversity in managed honey bees: reply to De la Rúa et al. (2013). Mol Ecol 22:3211–3215CrossRefPubMedGoogle Scholar
  11. MacDonald SE, Wilkie DM (1990) Yellow-nosed monkeys’ (Cercopithecus ascanius whitesidei) spatial memory in a simulated foraging environment. J Comp Psychol 104:382CrossRefGoogle Scholar
  12. Mench J, Andrew R (1986) Lateralization of a food search task in the domestic chick. Behav Neural Biol 46:107–114CrossRefPubMedGoogle Scholar
  13. Menzel R (1990) Learning, memory, and “cognition” in honey bees. In: Kesner RP, Olton DS (eds) Neurobiology of Comparative Cognition. Lawrence Erlbaum Associates, Hillsdale, pp 237–292Google Scholar
  14. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62CrossRefPubMedGoogle Scholar
  15. Menzel R, Brandt R, Gumbert A, Komischke B, Kunze J (2000) Two spatial memories for honey bee navigation. Proc R Soc Lond B Biol Sci 267:961–968CrossRefGoogle Scholar
  16. Menzel R, Geiger K, Joerges J, Müller U, Chittka L (1998) Bees travel novel homeward routes by integrating separately acquired vector memories. Anim Behav 55:139–152CrossRefPubMedGoogle Scholar
  17. Menzel R et al (2005) Honey bees navigate according to a map-like spatial memory. Proc Natl Acad Sci USA 102:3040–3045CrossRefPubMedGoogle Scholar
  18. Menzel R, Muller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404CrossRefPubMedGoogle Scholar
  19. Oades RD, Isaacson RL (1978) The development of food search behavior by rats: the effects of hippocampal damage and haloperidol. Behav Biol 24:327–337CrossRefPubMedGoogle Scholar
  20. Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142CrossRefGoogle Scholar
  21. Srinivasan M, Zhang S, Zhu H (1998) Honeybees link sights to smells. Nature 396:637–638CrossRefGoogle Scholar
  22. Team R (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2008. ISBN 3-900051-07-0Google Scholar
  23. von Frisch K (1967) The dance language and orientation of bees. Harvard University, CambridgeGoogle Scholar
  24. Whitfield CW et al (2006) Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci USA 103:16068–16075CrossRefPubMedGoogle Scholar
  25. Winston ML (1991) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  26. Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honey bee. Nature 364:238–240CrossRefPubMedGoogle Scholar
  27. Zayed A, Naeger N, Rodriguez-Zas S, Robinson G (2012) Common and novel transcriptional routes to behavioral maturation in worker and male honey bees. Genes Brain Behav 11:253–261CrossRefPubMedGoogle Scholar
  28. Zayed A, Robinson GE (2012) Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee. Annu Rev Genet 46:591–615CrossRefPubMedGoogle Scholar
  29. Zhang S, Bartsch K, Srinivasan M (1996) Maze learning by honeybees. Neurobiol Learn Mem 66:267–282CrossRefPubMedGoogle Scholar
  30. Zhang S, Lehrer M, Srinivasan M (1998a) Eye-specific learning of routes and “signposts” by walking honeybees. J Comp Physiol A 182:747–754CrossRefGoogle Scholar
  31. Zhang S, Lehrer M, Srinivasan M (1998b) Stimulus-conditioned sequence learning in honeybees. In: Proceedings of the 26th Göttingen neurobiology conference. Thieme, StuttgartGoogle Scholar
  32. Zhang S, Mizutani A, Srinivasan MV (2000) Maze navigation by honeybees: learning path regularity. Learn Mem 7:363–374CrossRefPubMedPubMedCentralGoogle Scholar
  33. Zhang SW, Lehrer M, Srinivasan MV (1999) Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol Learn Mem 72:180–201CrossRefPubMedGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  • N. Tsvetkov
    • 1
  • B. Madani
    • 1
  • L. Krimus
    • 1
  • S. E. MacDonald
    • 2
  • A. Zayed
    • 1
  1. 1.Department of BiologyYork UniversityTorontoCanada
  2. 2.Department of PsychologyYork UniversityTorontoCanada

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