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Double-edged heat: honeybee participation in a hot defensive bee ball reduces life expectancy with an increased likelihood of engaging in future defense

  • Yuta Yamaguchi
  • Atsushi Ugajin
  • Satoshi Utagawa
  • Masakazu Nishimura
  • Mitsuru Hattori
  • Masato Ono
Original Article

Abstract

Asian honeybees (Apis cerana) have evolved a thermal collective defense against the sympatric giant hornet (Vespa mandarinia) in which workers surround the predator en masse and produce heat up to 46 °C to kill it. This characteristic behavior is called “hot defensive bee ball formation.” Many studies have described the uniqueness and efficiency of this behavior; however, little attention has been paid to the potential cost to the honeybee. In this study, we focused on potential effects to bee ball-participating honeybees. We compared life expectancy of same-age ball-participating honeybees and nonparticipating honeybees and demonstrated that the life expectancy of the bee ball-participating honeybees was dramatically shortened. The 46 °C exposure also shortened the life expectancy of honeybees with induced expression of the heat shock protein gene, strongly implicating the increased temperature inside the bee ball in the deleterious effect on participating honeybees. We additionally found that bee ball-participating and then short-lived worker honeybees had a tendency to join a subsequent bee ball more aggressively. This tendency could mitigate accumulation of the short-lived worker honeybees within the colony, which otherwise would cause a severe reduction of honeybee colony activity.

Significance statement

Social insects have evolved unique anti-predator altruistic behaviors for colony defense. Evaluation of the potential cost of these behaviors provides valuable insight into their evolution. Asian honeybees (Apis cerana) exhibit a sophisticated collective defense (bee ball formation) against the sympatric giant hornet (Vespa mandarinia) whose rigid exoskeleton resists the common stinging attack of the honeybees, utilizing heat. We found that the high temperature inside the ball itself dramatically reduced honeybee longevity. Furthermore, bee ball-experienced honeybees were found to be more likely to engage in subsequent bee ball formation. Our results pointed out unavoidable cost for the honeybee colony associated with the use of heat and a “division of risk” strategy in the bee colony for minimizing the cost.

Keywords

Anti-predator behavior Hot defensive bee ball Life expectancy Heat shock protein Honeybee Hornet 

Notes

Acknowledgements

We are grateful to Mr. Tomio Yamaguchi for providing the honeybee colonies. We would like to thank Mr. Masaki Maruyama for his assistance in the bee ball experiments. Drs. Satoshi Miyazaki and Ryohei Kubo provided constructive comments on our study. We also thank Dr. James FA Traniello and two anonymous reviewers for their valuable comments on the manuscript.

Author’s contributions

YY, AU, SU, and MO conceived and designed the study. YY, SU, and MN carried out the behavioral experiments. AU performed the molecular lab work. YY and AU analyzed the data. AU and MH wrote the manuscript. YY and AU contributed equally to this work. All authors gave final approval for publication.

Funding

This work was supported in part by Japan Society for the Promotion of Science (JSPS) KAKENHI grant number JP14J12036 (Grant-in-Aid for JSPS Research Fellow, for AU).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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265_2018_2545_MOESM2_ESM.mp4 (14 mb)
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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Applied Entomology and Zoology, Graduate School of AgricultureTamagawa UniversityMachida, TokyoJapan
  2. 2.JT Biohistory Research HallTakatsuki-shi, OsakaJapan
  3. 3.College of AgricultureTamagawa UniversityMachida, TokyoJapan
  4. 4.Graduate School of Fisheries and Environmental SciencesNagasaki UniversityNagasaki CityJapan

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