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.
Spatial learning and memory Honey bee Behavioural state Apis mellifera
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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.
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
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
Chauvin C, Thierry B (2005) Tonkean macaques orient their food search from olfactory cues conveyed by conspecifics. Ethology 111:301–310CrossRefGoogle Scholar
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
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
Dyer FC, Berry NA, Richard AS (1993) Honey bee spatial memory: use of route-based memories after displacement. Anim Behav 45:1028–1030CrossRefGoogle Scholar
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
Harpur B et al (2015) Assessing patterns of admixture and ancestry in Canadian honey bees. Insectes Soc 62:479–489CrossRefGoogle Scholar
Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Mol Ecol 21:4414–4421CrossRefPubMedGoogle Scholar
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
MacDonald SE, Wilkie DM (1990) Yellow-nosed monkeys’ (Cercopithecus ascanius whitesidei) spatial memory in a simulated foraging environment. J Comp Psychol 104:382CrossRefGoogle Scholar
Mench J, Andrew R (1986) Lateralization of a food search task in the domestic chick. Behav Neural Biol 46:107–114CrossRefPubMedGoogle Scholar
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
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
von Frisch K (1967) The dance language and orientation of bees. Harvard University, CambridgeGoogle Scholar
Whitfield CW et al (2006) Genomic dissection of behavioral maturation in the honey bee. Proc Natl Acad Sci USA 103:16068–16075CrossRefPubMedGoogle Scholar
Winston ML (1991) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honey bee. Nature 364:238–240CrossRefPubMedGoogle Scholar
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
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