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Time-accuracy trade-off and task partitioning of hygienic behavior among honey bee (Apis mellifera) workers

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Abstract

Behavioral specialization and cooperation are fundamental in the organization and success of social groups. Honey bee workers display hygienic behavior, defined as the detection, uncapping, and removal of unhealthy brood. We present detailed analyses of behavioral specialization and task partitioning among hygienic worker bees, focusing on uncapping of brood cells and removal of the cells’ content in freeze-killed brood assays. We demonstrate specialization of hygienic workers on either uncapping or removal and task partitioning among multiple individuals. Speed of hygiene decreases with the number of behavioral instances, suggesting a time cost for cooperation of multiple individuals. Additional analyses of an individual agent-based simulation of hygienic removal of Varroa-mite-infested brood demonstrate that erroneous removal of healthy brood can be reduced by task partitioning due to collective decision-making. Combined, our results indicate a speed-accuracy trade-off in the collective performance of hygienic behavior: Hygienic behavior may take longer when many individuals contribute and specialize on different tasks, but this organization of work also can prevent costly mistakes. This trade-off may explain the observed combination of elite workers and numerous other workers that contribute only little.

Significance statement

Honey bees and other social animals form successful groups that are characterized by individual specialization on different tasks. Hygienic behavior of honey bees removes unhealthy brood from the nest and is important for the health of honey bee colonies. Here, we observed that individual worker bees specialize on either of the two main tasks involved in hygienic behavior: uncapping cells or removing brood. We also found that a few individuals perform the majority of the work and that the speed of hygienic behavior is higher when one individual works continuously instead of multiple individuals. Additionally, we show in computer simulations that the number of erroneous brood removals is decreased when separate workers contribute to the different aspects of hygienic behavior. Thus, our study indicates that a speed-accuracy trade-off might drive the evolution of task partitioning in hygienic behavior.

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Data availability

Behavioral data are available as online supplement. Biological materials were not preserved. The simulation code is also provided as online supplement.

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Acknowledgments

We would like to warmly thank all members of the REU program and the UNCG Social Insect Lab for their encouragement and feedback. Additionally, we appreciate the time and effort of our peer reviewers to improve the quality of this manuscript.

Funding

Financial support was provided by the US National Science Foundation (DMS 1659646) and the US Department of Agriculture (National Institute for Food and Agriculture, 2017-68004-26321). The funders had no role in designing the experiments or interpreting the results.

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Author notes

  1. Katherine R. Barrs

    Present address: Department of Biology, Department of Mathematical Sciences, Georgia Southern University, Statesboro, GA, USA

  2. M. Omar Ani

    Present address: Department of Chemistry, Rutgers University, New Brunswick, NJ, USA

  3. Kimberlyn K. Eversman

    Present address: Department of Mathematics, University of Tennessee, Knoxville, TN, USA

  4. Olav Rueppell

    Present address: Department of Biological Sciences, University of Alberta, CW 405 Biological Sciences Building, Edmonton, AB, T6G 2E9, Canada

  5. Katherine R. Barrs, M. Omar Ani and Kimberlyn K. Eversman contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of North Carolina, Greensboro, NC, USA

    Katherine R. Barrs, M. Omar Ani, Kimberlyn K. Eversman, Kaira M. Wagoner & Olav Rueppell

  2. Department of Mathematics and Statistics, University of North Carolina, Greensboro, NC, USA

    Jonathan T. Rowell

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  1. Katherine R. Barrs
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Contributions

KRB, MOA, KKE, and OR designed and planned the study. Empirical data collection was primarily performed by KRB and MOA, while the simulation was performed primarily by KKE and checked by JTR. Data analysis and interpretation were performed by KRB, MOA, KKE, KMW, and OR. All authors contributed to the writing of the manuscript, with a first version drafted by KRB, MOA, and KKE and the final version completed with major revisions from KMW and OR.

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Correspondence to Olav Rueppell.

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This work was exempt from institutional review and complies with all applicable laws of the USA. Great care was taken to not harm any bees unnecessarily.

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The authors declare that they have no conflict of interest.

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Communicated by D. Naug

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Barrs, K.R., Ani, M.O., Eversman, K.K. et al. Time-accuracy trade-off and task partitioning of hygienic behavior among honey bee (Apis mellifera) workers. Behav Ecol Sociobiol 75, 12 (2021). https://doi.org/10.1007/s00265-020-02940-y

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