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.
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.
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Abrol DP (2006) Defensive behaviour of Apis cerana F. against predatory wasps. J Apicult Sci 50:39–46
Clayton DF (2000) The genomic action potential. Neurobiol Learn Mem 74:185–216
Döke MA, Frazier M, Grozinger CM (2015) Overwintering honey bees: biology and management. Curr Opin Insect Sci 10:185–193. https://doi.org/10.1016/j.cois.2015.05.014
Elekonich MM (2009) Extreme thermotolerance and behavioral induction of 70-kDa heat shock proteins and their encoding genes in honey bees. Cell Stress Chaperones 14:219–226. https://doi.org/10.1007/s12192-008-0063-z
Epel ES, Lithgow GJ (2014) Stress biology and aging mechanisms: toward understanding the deep connection between adaptation to stress and longevity. J Gerontol A Biol Sci Med Sci 69:S10–S16. https://doi.org/10.1093/gerona/glu055
Even N, Devaud JM, Barron AB (2012) General stress responses in the honey bee. Insects 3:1271–1298. https://doi.org/10.3390/insects3041271
Fahrbach SE (2006) Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209–232. https://doi.org/10.1146/annurev.ento.51.110104.150954
Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15:599–606. https://doi.org/10.1016/j.conb.2005.08.018
Heinrich B (1980) Mechanisms of body-temperature regulation in honeybees, Apis mellifera. J Exp Biol 85:61–72
Hoso M (2012) Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail. Proc Biol Sci 279:4811–4816. https://doi.org/10.1098/rspb.2012.1943
Johnson BR (2003) Organization of work in the honeybee: a compromise between division of labour and behavioural flexibility. Proc R Soc Lond B 270:147–152. https://doi.org/10.1098/rspb.2002.2207
Johnson BR (2010) Division of labor in honeybees: form, function, and proximate mechanisms. Behav Ecol Sociobiol 64:305–316. https://doi.org/10.1007/s00265-009-0874-7
Johnson EC (2016) Stressed-out insects II. Physiology, behavior, and neuroendocrine circuits mediating stress responses. In: Pfaff DW, Joëls M (eds) Hormones, brain and behavior. Academic Press, San Diego, pp 465–481
Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 25:577–586. https://doi.org/10.1016/S0149-7634(01)00042-2
King AM, MacRae TH (2015) Insect heat shock proteins during stress and diapause. Annu Rev Entomol 60:59–75. https://doi.org/10.1146/annurev-ento-011613-162107
Koo J, Son TG, Kim SY, Lee KY (2015) Differential responses of Apis mellifera heat shock protein genes to heat shock, flower-thinning formulations, and imidacloprid. J Asia-Pacific Entomol 18:583–589. https://doi.org/10.1016/j.aspen.2015.06.011
Li-Byarlay H, Rittschof CC, Massey JH, Pittendrigh BR, Robinson GE (2014) Socially responsive effects of brain oxidative metabolism on aggression. Proc Natl Acad Sci U S A 111:12533–12537. https://doi.org/10.1073/pnas.1412306111
Loebrich S, Nedivi E (2009) The function of activity-regulated genes in the nervous system. Physiol Rev 89:1079–1103. https://doi.org/10.1152/physrev.00013.2009
Lutz CC, Robinson GE (2013) Activity-dependent gene expression in honey bee mushroom bodies in response to orientation flight. J Exp Biol 216:2031–2038. https://doi.org/10.1242/jeb.084905
Matsuura M (1988) Ecological study on vespine wasps (Hymenoptera: Vespidae) attacking honeybee colonies. I. Seasonal changes in the frequency of visits to apiaries by vespine wasps and damage inflicted, especially in the absence of artificial protection. Appl Entomol Zool 23:428–440
Nouvian M, Reinhard J, Giurfa M (2016) The defensive response of the honeybee Apis mellifera. J Exp Biol 219:3505–3517. https://doi.org/10.1242/jeb.143016
Ono M, Okada I, Sasaki M (1987) Heat production by balling in the Japanese honeybee, Apis cerana japonica as a defensive behavior against the hornet, Vespa simillima xanthoptera (Hymenoptera: Vespidae). Experientia 43:1031–1032
Ono M, Igarashi T, Ohno E, Sasaki M (1995) Unusual thermal defense by a honeybee against mass attack by hornets. Nature 377:334–336. https://doi.org/10.1038/377334a0
Park D, Jung JW, Choi B-S, Jayakodi M, Lee J, Lim J, Yu Y, Choi YS, Lee ML, Park Y, Choi IY, Yang TJ, Edwards OR, Nah G, Kwon HW (2015) Uncovering the novel characteristics of Asian honeybee, Apis cerana, by whole genome sequencing. BMC Genomics 16(1). https://doi.org/10.1186/1471-2164-16-1
Reeder DM, Kramer KM (2005) Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86:225–235. https://doi.org/10.1644/BHE-003.1
Roberts SP, Harrison JF (1999) Mechanisms of thermal stability during flight in the honeybee Apis mellifera. J Exp Biol 202:1523–1533
Roberts SP, Elekonich MM (2005) Muscle biochemistry and the ontogeny of flight capacity during behavioral development in the honey bee, Apis mellifera. J Exp Biol 208:4193–4198. https://doi.org/10.1242/jeb.01862
Shpigler HY, Saul MC, Murdoch EE, Cash-Ahmed AC, Seward CH, Sloofman L, Chandrasekaran S, Sinha S, Stubbs LJ, Robinson GE (2017) Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees. Genes Brain Behav 16:579–591. https://doi.org/10.1111/gbb.12379
Sugahara M, Sakamoto F (2009) Heat and carbon dioxide generated by honeybees jointly act to kill hornets. Naturwissenschaften 96:1133–1136. https://doi.org/10.1007/s00114-009-0575-0
Sugahara M, Nishimura Y, Sakamoto F (2012) Differences in heat sensitivity between Japanese honeybees and hornets under high carbon dioxide and humidity conditions inside bee balls. Zool Sci 29:30–36. https://doi.org/10.2108/zsj.29.30
Tan K, Hepburn HR, Radloff SE, Yusheng Y, Yiqiu L, Danyin Z, Neumann P (2005) Heat-balling wasps by honeybees. Naturwissenschaften 92:492–495. https://doi.org/10.1007/s00114-005-0026-5
Tan K, Li H, Yang MX, Hepburn HR, Radloff SE (2010) Wasp hawking induces endothermic heat production in guard bees. J Insect Sci 10(142):1–6. https://doi.org/10.1673/031.010.14102
Tan K, Wang Z, Chen W, Hu Z, Oldroyd BP (2013) The ‘I see you’ prey-predator signal of Apis cerana is innate. Naturwissenschaften 100:245–248. https://doi.org/10.1007/s00114-013-1019-4
Tan K, Dong S, Li X, Liu X, Wang C, Li J, Nieh JC (2016) Honey bee inhibitory signaling is tuned to threat severity and can act as a colony alarm signal. PLoS Biol 14:e1002423. https://doi.org/10.1371/journal.pbio.1002423
Ugajin A, Kiya T, Kunieda T, Ono M, Yoshida T, Kubo T (2012) Detection of neural activity in the brains of Japanese honeybee workers during the formation of a “hot defensive bee ball”. PLoS One 7:e32902. https://doi.org/10.1371/journal.pone.0032902
Ugajin A, Kunieda T, Kubo T (2013) Identification and characterization of an Egr ortholog as a neural immediate early gene in the European honeybee (Apis mellifera L.). FEBS Lett 587:3224–3230. https://doi.org/10.1016/j.febslet.2013.08.014
Ugajin A, Uchiyama H, Miyata T, Sasaki T, Yajima S, Ono M (2018) Identification and initial characterization of novel neural immediate early genes possibly differentially contributing to foraging-related learning and memory processes in the honeybee. Insect Mol Biol 27:154–165. https://doi.org/10.1111/imb.12355
Wang Z, Qu Y, Dong S, Wen P, Li J, Tan K, Menzel R (2016) Honey bees modulate their olfactory learning in the presence of hornet predators and alarm component. PLoS One 11:e0150399. https://doi.org/10.1371/journal.pone.0150399
Woyciechowski M, Moroń D (2009) Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insect Soc 56:193–201. https://doi.org/10.1007/s00040-009-0012-6
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.
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).
Conflict of interest
The authors declare that they have no conflict of interest.
Communicated by O. Rueppell
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Yamaguchi, Y., Ugajin, A., Utagawa, S. et al. Double-edged heat: honeybee participation in a hot defensive bee ball reduces life expectancy with an increased likelihood of engaging in future defense. Behav Ecol Sociobiol 72, 123 (2018). https://doi.org/10.1007/s00265-018-2545-z
- Anti-predator behavior
- Hot defensive bee ball
- Life expectancy
- Heat shock protein