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Free-flying honeybees extrapolate relational size rules to sort successively visited artificial flowers in a realistic foraging situation

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Abstract

Learning and applying relational concepts to solve novel tasks is considered an indicator of cognitive-like ability. It requires the abstraction of relational concepts to different objects independent to the physical nature of the individual objects. Recent research has revealed the honeybee’s ability to rapidly learn and manipulate relations between visual stimuli such as ‘same/different’, ‘above/below’, or ‘larger/smaller’ despite having a miniature-sized brain. While honeybees can solve problems using rule-based relative size comparison, it remains unresolved as to whether bees can apply size rules when stimuli are encountered successively, which requires reliance on working memory for stimuli comparison. Additionally, the potential ability of bees to extrapolate acquired information to novel sizes beyond training sets remains to be investigated. We tested whether individual free-flying honeybees could learn ‘larger/smaller’ size rules when visual stimuli were presented successively, and whether such rules could then be extrapolated to novel stimulus sizes. Honeybees were individually trained to a set of four sizes such that individual elements might be correct, or incorrect, depending upon the alternative stimulus. In a learning test, bees preferred the correct size relation for their respective learning group. Bees were also able to successfully extrapolate the learnt relation during transfer tests by maintaining the correct size relationships when considering either two smaller, or two larger, novel stimulus sizes. This performance demonstrates that an insect operating in a complex environment has sufficient cognitive capacity to learn rules that can be abstracted to novel problems. We discuss the possible learning mechanisms which allow their success.

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Acknowledgements

We thank Assoc. Prof. Devi Stuart-Fox for her comments on multiple drafts of the manuscript. We thank Dr. Mani Shrestha for his help measuring spectral properties of the stimuli. Adrian G Dyer acknowledges Australian Research Council (ARC) 130100015. We also wish to acknowledge the three anonymous reviewers and Professor Ken Cheng for their expert advice on previous versions of the manuscript.

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Authors and Affiliations

  1. Bio-inspired Digital Sensing (BIDS) Lab, School of Media and Communication, RMIT University, Melbourne, VIC, Australia

    Scarlett R. Howard, Jair Garcia & Adrian G. Dyer

  2. School of Biosciences, University of Melbourne, Parkville, VIC, Australia

    Scarlett R. Howard

  3. Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative (CBI), Université de Toulouse, CNRS, UPS, Toulouse, France

    Aurore Avarguès-Weber

  4. Department of Physiology, Monash University, Clayton, VIC, Australia

    Adrian G. Dyer

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  1. Scarlett R. Howard
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Contributions

Scarlett Howard was involved in the design of the experiment, data collection, data analysis and interpretation, and drafted the manuscript. Aurore Avarguès-Weber was involved in the experimental design, interpretation of data, and drafting of the manuscript. Jair Garcia was involved in the data analysis and drafting of the manuscript. Adrian Dyer was involved in the design of the experiment, data collection, data analysis, and drafting the manuscript. All authors gave final approval for submission.

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Correspondence to Scarlett R. Howard.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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This video shows a honeybee at 0.25× original speed aborting a choice for a 3 × 3 cm stimulus in the learning test at 3.73 s, aborting a choice for a 1 × 1 cm stimulus in the transfer test to smaller stimuli at 10.13 s, and aborting a choice for a 7 × 7 cm stimulus during the transfer test to larger stimuli at 21.9 s (MP4 2899 kb)

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Howard, S.R., Avarguès-Weber, A., Garcia, J. et al. Free-flying honeybees extrapolate relational size rules to sort successively visited artificial flowers in a realistic foraging situation. Anim Cogn 20, 627–638 (2017). https://doi.org/10.1007/s10071-017-1086-6

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