Honey bee workers generate low-frequency vibrations that are reliable indicators of their activity level

Abstract

In social insects, the tuning of activity levels among different worker task groups, which constitutes a fundamental basis of colony organization, relies on the exchange of reliable information on the activity level of individuals. The underlying stimuli, however, have remained largely unexplored so far. In the present study, we describe low-frequency thoracic vibrations generated by honey bee workers (Apis mellifera) within the colony, whose velocity amplitudes and main frequency components significantly increased with the level of an individual’s activity. The characteristics of these vibrations segregated three main activity level-groups: foragers, active hive bees, and inactive hive bees. Nectar foragers, moreover, modulated their low-frequency vibrations during trophallactic food unloading to nestmates according to the quality of the collected food. Owing to their clear association with the activity level of an individual and their potential perceptibility during direct contacts, these low-frequency thoracic vibrations are candidate stimuli for providing unambiguous local information on the motivational status of honey bee workers.

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References

  1. Anderson C, Ratnieks FLW (1999) Worker allocation in insect societies: coordination of nectar foragers and nectar receivers in honey bee (Apis mellifera) colonies. Behav Ecol Sociobiol 46:73–81. https://doi.org/10.1007/s002650050595

    Article  Google Scholar 

  2. Arenas A, Fernández VM, Farina WM (2008) Floral scents experienced within the colony affect long-term foraging preferences in honeybees. Apidologie 39:714–722. https://doi.org/10.1051/apido:2008053

    Article  Google Scholar 

  3. Autrum H, Schneider W (1948) Vergleichende Untersuchungen über den Erschütterungssinn der Insekten. Z Vergl Physiol 31:77–88. https://doi.org/10.1007/BF00333879

    Article  CAS  Google Scholar 

  4. Balbuena MS, Molinas J, Farina WM (2012) Honeybee recruitment to scented food sources: correlations between in-hive social interactions and foraging decision making. Behav Ecol Sociobiol 66:445–452. https://doi.org/10.1007/s00265-011-1290-3

    Article  Google Scholar 

  5. Bastian J, Esch H (1970) The nervous control of the indirect flight muscles of the honey bee. Z vergl Physiol 67:307–324. https://doi.org/10.1007/BF00340954

    Article  Google Scholar 

  6. Bonabeau E, Theraulaz G, Deneubourg JL, Aron S, Camazine S (1997) Self-organization in social insects. Trends Ecol Evol 15:188–193. https://doi.org/10.1016/S0169-5347(97)01048-3

    Article  Google Scholar 

  7. Camazine S, Deneubourg JL, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2003) Self-organization in biological systems. Princeton University Press, Princeton

    Google Scholar 

  8. De Marco RJ, Farina WM (2001) Changes in food source profitability affect the trophallactic and dance behavior of forager honeybees (Apis mellifera L.). Behav Ecol Sociobiol 50:441–449. https://doi.org/10.1007/s002650100382

    Article  Google Scholar 

  9. Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744. https://doi.org/10.1007/s003590050296

    Article  Google Scholar 

  10. Esch H (1960) Über die Körpertemperaturen und den Wärmehaushalt von Apis mellifica. Z vergl Physiol 43:305–335. https://doi.org/10.1007/BF00298066

    Article  Google Scholar 

  11. Esch H, Bastian J (1968) Mechanical and electrical activity in the indirect flight muscles of the honey bee. Z Vergl Physiol 58:429–440. https://doi.org/10.1007/BF00343515

    Article  Google Scholar 

  12. Esch H, Nachtigall W, Kogge SN (1975) Correlations between aerodynamic output, electrical activity in the indirect flight muscles and wing positions of bees flying in a servomechanically controlled wind tunnel. J Comp Physiol 100:147–159. https://doi.org/10.1007/BF00613966

    Article  Google Scholar 

  13. Esch H, Goller F, Heinrich B (1991) How do bees shiver? Naturwissenschaften 78:325–328. https://doi.org/10.1007/BF01221422

    Article  CAS  PubMed  Google Scholar 

  14. Farina WM (1996) Food-exchange by foragers in the hive—a means of communication among honey bees? Behav Ecol Sociobiol 38:59–64. https://doi.org/10.1007/s002650050217

    Article  Google Scholar 

  15. Farina WM (2000) The interplay between dancing and trophallactic behavior in the honey bee Apis mellifera. J Comp Physiol A 186:239–245. https://doi.org/10.1007/s003590050424

    Article  CAS  PubMed  Google Scholar 

  16. Farina WM, Wainselboim A (2001) Changes in the thoracic temperature of honey bees while receiving nectar from foragers collecting at different reward rates. J Exp Biol 204:1653–1658

    CAS  PubMed  Google Scholar 

  17. Farina WM, Grüter C, Acosta LE, Mc Cabe S (2007) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:55–60. https://doi.org/10.1007/s00114-006-0157-3

    Article  CAS  PubMed  Google Scholar 

  18. Germ M, Stabentheiner A, Kastberger G (1997) Seasonal and daily variation of honeybee dancing temperature under constant feeding conditions. Apidologie 28:385–398. https://doi.org/10.1051/apido:19970606

    Article  Google Scholar 

  19. Goller F, Esch HE (1991) Oxygen consumption and flight muscle activity during heating in workers and drones of Apis mellifera. J Comp Physiol B 161:61–67. https://doi.org/10.1007/BF00258747

    Article  Google Scholar 

  20. Grüter C, Keller L (2016) Inter-caste communication in social insects. Curr Opin Neurobiol 38:6–11. https://doi.org/10.1016/j.conb.2016.01.002

    Article  CAS  PubMed  Google Scholar 

  21. Heinrich B, Kammer AE (1973) Activation of the fibrillar muscles in the bumblebee during warm-up, stabilization of thoracic temperature and flight. J Exp Biol 58:677–688

    Google Scholar 

  22. Heran H (1952) Untersuchungen über den Temperatursinn der Honigbiene (Apis mellifica) unter besonderer Berücksichtigung der Wahrnehmung strahlender Wärme. Z Vergl Physiol 34:179–206. https://doi.org/10.1007/BF00339537

    Article  Google Scholar 

  23. Heran H (1959) Wahrnehmung und Regelung der Flugeigengeschwindigkeit bei Apis mellifica L. Z vergl Physiol 42:103–163. https://doi.org/10.1007/BF00298733

    Article  Google Scholar 

  24. Hrncir M, Jarau S, Zucchi R, Barth FG (2004) Thorax vibrations of a stingless bee (Melipona seminigra). II. Dependence on sugar concentration. J Comp Physiol A 190:549–560. https://doi.org/10.1007/s00359-004-0515-6

    CAS  Article  Google Scholar 

  25. Hrncir M, Barth FG, Tautz J (2006a) Vibratory and airborne sound-signals in bee communication. In: Drosopoulos S, Claridge M (eds) Insect sounds and communication: physiology, behaviour, ecology, and evolution. CRC Press, Boca Raton, pp 421–436

    Google Scholar 

  26. Hrncir M, Schmidt VM, Schorkopf DLP, Jarau S, Zucchi R, Barth FG (2006b) Vibrating the food receivers: a direct way of signal transmission in stingless bees (Melipona seminigra). J Comp Physiol A 192:879–887. https://doi.org/10.1007/s00359-006-0123-8

    Article  Google Scholar 

  27. Hrncir M, Schorkopf DLP, Schmidt VM, Zucchi R, Barth FG (2008) The sound field generated by tethered stingless bees (Melipona scutellaris): inferences on its potential as a recruitment mechanism inside the hive. J Exp Biol 211:686–698

    Article  PubMed  Google Scholar 

  28. Hrncir M, Maia-Silva C, Mc Cabe SI, Farina WM (2011) The recruiter’s excitement – features of thoracic vibrations during the honey bee’s waggle dance related to food source profitability. J Exp Biol 214:4055–4064. https://doi.org/10.1007/s00359-006-0123-8

    Article  Google Scholar 

  29. Hunt JH, Richard FJ (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417. https://doi.org/10.1007/s00040-013-0311-9

    Article  Google Scholar 

  30. Johnson BR (2010a) Task partitioning in honey bees: the roles of signals and cues in group-level coordination of action. Behav Ecol 21:1373–1379. https://doi.org/10.1093/beheco/arq138

    Article  Google Scholar 

  31. Johnson BR (2010b) 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

    Article  PubMed  Google Scholar 

  32. Kammer AE, Heinrich B (1974) Metabolic rates related to muscle activity in bumblebees. J Exp Biol 61:219–227

    CAS  PubMed  Google Scholar 

  33. Kather R, Drijfhout FP, Martin SJ (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37:205–212. https://doi.org/10.1007/s10886-011-9909-4

    Article  CAS  PubMed  Google Scholar 

  34. Kilpinen O, Storm J (1997) Biophysics of the subgenual organ of the honeybee, Apis mellifera. J Comp Physiol A 181:309–318. https://doi.org/10.1007/s003590050117

    Article  Google Scholar 

  35. Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L.). Z Vergl Physiol 48:587–623. https://doi.org/10.1007/BF00333743

    Article  Google Scholar 

  36. Lewis LA, Schneider SS, De-Grandi-Hoffmann G (2002) Factors influencing the selection of recipients by workers performing vibration signals in colonies of the honeybee, Apis mellifera. Anim Behav 63:361–367. https://doi.org/10.1006/anbe.2001.1894

    Article  Google Scholar 

  37. Lindauer M (1954) Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z Vergl Physiol 36:391–432. https://doi.org/10.1007/BF00345028

    Article  Google Scholar 

  38. Martinez A, Farina WM (2008) Honeybees modify their gustatory responsiveness after receiving nectar from foragers within the hive. Behav Ecol Sociobiol 62:529–535. https://doi.org/10.1007/s00265-007-0477-0

    Article  Google Scholar 

  39. Mc Cabe SI, Hrncir M, Farina WM (2015) Vibrating donor-partners during trophallaxis modulate associative learning ability of food receivers in the stingless bee Melipona quadrifasciata. Learn Motiv 50:11–21. https://doi.org/10.1016/j.lmot.2014.10.005

    Article  Google Scholar 

  40. Michelsen A, Towne WF, Kirchner WH, Kryger P (1987) The acoustic near field of a dancing honeybee. J Comp Physiol A 161:633–643. https://doi.org/10.1007/BF00605005

    Article  Google Scholar 

  41. Moauro MA, Balbuena MS, Farina WM (2018) Assessment of appetitive behavior in honey bee dance followers. Front Behav Neurosci 12:74. https://doi.org/10.3389/fnbeh.2018.00074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Moritz RFA, Fuchs S (1998) Organization of honey bee colonies: Characteristics and consequences of a superorganism concept. Apidologie 29:7–21. https://doi.org/10.1051/apido:19980101

    Article  Google Scholar 

  43. Pankiw T, Nelson M, Page RE, Fondrk MK (2004) The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality. Behav Ecol Sociobiol 55:286–292. https://doi.org/10.1007/s00265-003-0714-0

    Article  Google Scholar 

  44. Pennycuick CJ, Rezende MA (1984) The specific power output of aerobic muscle, related to the power density of mitochondria. J Exp Biol 108:377–392

    Google Scholar 

  45. Pírez N, Farina WM (2004) Nectar-receiver behavior in relation to the reward rate experienced by foraging honeybees. Behav Ecol Sociobiol 55:574–582. https://doi.org/10.1007/s00265-003-0749-2

    Article  Google Scholar 

  46. Sadler N, Nieh JC (2011) Honey bee forager thoracic temperature inside the nest is tuned to broad-scale differences in recruitment motivation. J Exp Biol 214:469–475. https://doi.org/10.1242/jeb.049445

    Article  PubMed  Google Scholar 

  47. Sandeman DC, Tautz J, Lindauer M (1996) Transmission of vibration across honeycombs and its detection by bee leg receptors. J Exp Biol 199:2585–2594

    CAS  PubMed  Google Scholar 

  48. Scheiner R, Page RE, Erber J (2001) Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav Brain Res 120:67–73. https://doi.org/10.1016/S0166-4328(00)00359-4

    Article  CAS  PubMed  Google Scholar 

  49. Schneider SS, Lewis LA (2004) The vibration signal, modulatory communication and the organization of labor in honey bees, Apis mellifera. Apidologie 35:117–131. https://doi.org/10.1051/apido:2004006

    Article  Google Scholar 

  50. Seeley TD (1989a) The honey bee colony as a superorganism. Am Sci 77:546–553

    Google Scholar 

  51. Seeley TD (1989b) Social foraging in honey bees: how nectar foragers assess their colony’s nutritional status. Behav Ecol Sociobiol 24:181–199. https://doi.org/10.1007/BF00292101

    Article  Google Scholar 

  52. Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80. https://doi.org/10.1051/apido:19980104

    Article  Google Scholar 

  53. Seeley TD, Weidenmüller A, Kühnholz S (1998) The shaking signal of the honey bee informs workers to prepare for greater activity. Ethology 104:10–26. https://doi.org/10.1111/j.1439-0310.1998.tb00026.x

    Article  Google Scholar 

  54. Seeley TD, Mikheyev AS, Pagano GJ (2000) Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability. J Comp Physiol A 186:813–819. https://doi.org/10.1007/s003590000134

    Article  CAS  PubMed  Google Scholar 

  55. Slone JD, Stout TL, Huang ZY, Schneider SS (2012) The influence of drone physical condition on the likelihood of receiving vibration signals from worker honey bees, Apis mellifera. Insect Soc 59:101–107. https://doi.org/10.1007/s00040-011-0195-5

    Article  Google Scholar 

  56. Stabentheiner A, Hagmüller K (1991) Sweet food means “hot dancing” in honeybees. Naturwissenschaften 78:471–473. https://doi.org/10.1007/BF01134389

    Article  Google Scholar 

  57. Stabentheiner A, Kovac H, Hagmüller K (1995) Thermal behavior of round and wagtail dancing honeybees. J Comp Physiol B 165:433–444. https://doi.org/10.1007/BF00261297

    Article  Google Scholar 

  58. Stabentheiner A, Vollmann J, Kovac H, Crailsheim K (2003) Oxygen consumption and body temperature of active and resting honeybees. J Insect Physiol 49:881–889. https://doi.org/10.1016/S0022-1910(03)00148-3

    Article  CAS  PubMed  Google Scholar 

  59. Staudacher EM, Gebhardt M, Dürr V (2005) Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv Insect Physiol 32:49–205. https://doi.org/10.1016/S0065-2806(05)32002-9

    Article  CAS  Google Scholar 

  60. Thom C, Gilley DC, Hooper J, Esch HE (2007) The scent of the waggle dance. PLoS Biol 5:e228. https://doi.org/10.1371/journal.pbio.0050228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Tsujiuchi S, Sivan-Loukianova E, Eberl DF, Kitagawa Y, Kadowaki T (2007) Dynamic range compression in the honey bee auditory system toward waggle dance sounds. PLoS One 2:e234. https://doi.org/10.1371/journal.pone.0000234

    Article  PubMed  PubMed Central  Google Scholar 

  62. Waddington KD, Kirchner WH (1992) Acoustical and behavioral correlates of the profitability of food sources in honey bee round dances. Ethology 92:1–6. https://doi.org/10.1111/j.1439-0310.1992.tb00945.x

    Article  Google Scholar 

  63. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

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Acknowledgements

The experiments complied with the “Principles of Animal Care”, publication No. 86-23, revised 1985 by the National Institute of Health, and with the current laws of the country in which the experiments were performed. The study was financially supported by the Brazilian Science Funds FAPESP [2006/50809-7] and CNPq [304722/2010-3] to MH, and funding of ANPCYT (PICT 2016 2084), the University of Buenos Aires (UBACYT 2018 20020170100078BA), CONICET (PIP 112-201501-00633) and a Guggenheim fellowship to WMF. We would like to thank Prof. Friedrich G. Barth and the University of Vienna-Austria for loaning the laser-vibrometer used for recording the bees’ low-frequency vibrations, and two anonymous referees for valuable comments on the manuscript.

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Hrncir, M., Maia-Silva, C. & Farina, W.M. Honey bee workers generate low-frequency vibrations that are reliable indicators of their activity level. J Comp Physiol A 205, 79–86 (2019). https://doi.org/10.1007/s00359-018-1305-x

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Keywords

  • Social insects
  • Apis mellifera
  • Vibratory communication
  • Mechanical cues
  • Motivational state