Skip to main content

Circadian Rhythms and Sleep in Honey Bees

  • Chapter
  • First Online:
Honeybee Neurobiology and Behavior

Abstract

The circadian clock of the honey bee is involved in complex behaviors and is socially regulated. Initial molecular characterization suggests that in many ways the clock of the bee is more similar to mammals than to Drosophila. Foragers rely on the circadian clock to anticipate day–night fluctuations in their environment, time visits to flowers, and for time compensation when referring to the sun in sun-compass orientation and dance language communication. Both workers and queens show plasticity in circadian rhythms. In workers, circadian rhythms are influenced by task specialization and regulated by direct contact with the brood; nurse bees tend the brood around the clock with no circadian rhythms in behavior or clock gene expression. An important function of the circadian clock is the regulation of sleep. Bees show a clear sleep state with a characteristic posture, reduced muscle tonus, and elevated response threshold. Honey bee sleep is a dynamic process with common transitions between stages of deep and light sleep. The sleep stages of workers active around-the-clock are overall similar to foragers. Sleep deprivation leads to an increase in the expression of sleep characteristics the following day, and may interfere with some learning paradigms. This review shows that the honey bee is an excellent model with which to study circadian rhythms and sleep in an ecologically and socially relevant context. Future research needs to deepen our understanding of these fascinating behaviors, reveal their neuronal and molecular bases, and explore their interactions with other physiological processes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

FS:

First sleep stage

MB:

Mushroom body

mRNA:

messenger RNA

OL:

Optic lobe

SS:

Second sleep stage

TS:

Third sleep stage

References

  1. Allada R, Siegel JM (2008) Unearthing the phylogenetic roots of sleep. Curr Biol 18:R670–R679

    Article  PubMed  CAS  Google Scholar 

  2. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6:544–556

    Article  PubMed  CAS  Google Scholar 

  3. Bloch G (2009) Plasticity in the circadian clock and the temporal organization of insect societies. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, pp 402–432

    Google Scholar 

  4. Bloch G (2010) The social clock of the honeybee. J Biol Rhythm 25:307–317

    Article  Google Scholar 

  5. Bloch G, Robinson GE (2001) Reversal of honey bee behavioural rhythms. Nature 410:1048

    Article  PubMed  CAS  Google Scholar 

  6. Bloch G, Toma DP, Robinson GE (2001) Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J Biol Rhythm 16:444–456

    Article  CAS  Google Scholar 

  7. Bloch G, Solomon SM, Robinson GE, Fahrbach SE (2003) Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honey bee (Apis mellifera): age- and time-related plasticity. J Comp Neurol 464:269–284

    Article  PubMed  CAS  Google Scholar 

  8. Bloch G, Rubinstein CD, Robinson GE (2004) Period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type. Insect Biochem Mol Biol 34:879–891

    Article  PubMed  CAS  Google Scholar 

  9. Cirelli C (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci 10:549–560

    Article  PubMed  CAS  Google Scholar 

  10. Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6:1605–1611

    Article  CAS  Google Scholar 

  11. Dave AS, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290:812–816

    Article  PubMed  CAS  Google Scholar 

  12. Dunlap. JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer, Sunderland, 382 p

    Google Scholar 

  13. Eban-Rothschild AD, Bloch G (2008) Differences in the sleep architecture of forager and young honey bees (Apis mellifera). J Exp Biol 211:2408–2416

    Article  PubMed  Google Scholar 

  14. Hendricks C, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129–138

    Article  PubMed  CAS  Google Scholar 

  15. Hussaini SA, Bogusch L, Landgraf T, Menzel R (2009) Sleep deprivation affects extinction but not acquisition memory in honey bees. Learn Mem 16:698–705

    Article  PubMed  Google Scholar 

  16. Johnson JN, Hardgrave E, Gill C, Moore D (2010) Absence of consistent diel rhythmicity in mated honey bee queen behavior. J Insect Physiol 56:761–773

    Article  PubMed  CAS  Google Scholar 

  17. Joiner WJ, Crocker A, White BH, Sehgal A (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757–760

    Article  PubMed  CAS  Google Scholar 

  18. Kaiser W (1988) Busy bees need rest, too – behavioral and electomyographical sleep signs in honey bees. J Comp Physiol A 163:565–584

    Article  Google Scholar 

  19. Kaiser W, Steiner-Kaiser J (1983) Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301:707–709

    Article  PubMed  CAS  Google Scholar 

  20. Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste-dependent sleep of worker honey bees. J Exp Biol 211:3028–3040

    Article  PubMed  Google Scholar 

  21. Kleinhenz M, Bujok B, Fuchs S, Tautz H (2003) Hot bees in empty broodnest cells: heating from within. J Exp Biol 206:4217–4231

    Article  PubMed  Google Scholar 

  22. Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313–339

    Article  Google Scholar 

  23. Martinez-Gonzalez D, Lesku JA, Rattenborg NC (2008) Increased EEG spectral power density during sleep following short-term sleep deprivation in pigeons (Columba livia): evidence for avian sleep homeostasis. J Sleep Res 17:140–153

    Article  PubMed  Google Scholar 

  24. McCluskey ES (1992) Periodicity and diversity in ant mating flights. Comp Biochem Physiol 103:241–243

    Article  CAS  Google Scholar 

  25. Menzel R, Leboulle G, Eisenhardt D (2006) Small brains, bright minds. Cell 124:237–239

    Article  PubMed  CAS  Google Scholar 

  26. Mignot E (2008) Why we sleep: the temporal organization of recovery. PLoS Biol 6:661–669

    Article  CAS  Google Scholar 

  27. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857

    Article  CAS  Google Scholar 

  28. Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160

    Article  Google Scholar 

  29. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12:1934–1940

    Article  PubMed  CAS  Google Scholar 

  30. Pitman JL, McGill JJ, Keegan KP, Allada R (2006) A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441:753–756

    Article  PubMed  CAS  Google Scholar 

  31. Prober DA, Rihel J, Onah AA, Sung RJ, Schier AF (2006) Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J Neurosci 26:13400–13410

    Article  PubMed  CAS  Google Scholar 

  32. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV, Pack AI (2008) Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451:569–U6

    Article  PubMed  CAS  Google Scholar 

  33. Ramon F, Hernandez-Falcon J, Nguyen B, Bullock TH (2004) Slow wave sleep in crayfish. Proc Natl Acad Sci USA 101:11857–11861

    Article  PubMed  CAS  Google Scholar 

  34. Roth TC, Rattenborg NC, Pravosudov VV (2010) The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation. Philos Trans R Soc B Biol Sci 365:945–959

    Article  Google Scholar 

  35. Rubin EB, Shemesh Y, Cohen M, Elgavish S, Robertson HM, Bloch G (2006) Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res 16:1352–1365

    Article  PubMed  CAS  Google Scholar 

  36. Sauer S, Herrmann E, Kaiser W (2004) Sleep deprivation in honey bees. J Sleep Res 13:145–152

    Article  PubMed  Google Scholar 

  37. Sauer S, Kinkelin M, Herrmann E, Kaiser W (2003) The dynamics of sleep-like behaviour in honey bees. J Comp Physiol A 189:599–607

    Article  PubMed  CAS  Google Scholar 

  38. Schmolz E, Hoffmeister D, Lamprecht I (2002) Calorimetric investigations on metabolic rates and thermoregulation of sleeping honey bee s (Apis mellifera carnica). Thermochim Acta 382:221–227

    Article  CAS  Google Scholar 

  39. Schuppe H (1995) Rhythmic brain activity in sleeping bees. Wien Med Wochenschr 145:463–4

    PubMed  CAS  Google Scholar 

  40. Sharma VK, Lone SR, Goel A (2004) Clocks for sex: loss of circadian rhythms in ants after mating? Naturwissenschaften 91:334–337

    PubMed  CAS  Google Scholar 

  41. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837

    Article  PubMed  CAS  Google Scholar 

  42. Shemesh Y, Cohen M, Bloch G (2007) Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honey bees. FASEB J 21:2304–2311

    Article  PubMed  CAS  Google Scholar 

  43. Shemesh Y, Eban-Rothschild AD, Cohen M, Bloch G (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J Neurosci 30:12517–12525

    Article  PubMed  CAS  Google Scholar 

  44. Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264–1271

    Article  PubMed  CAS  Google Scholar 

  45. Tobler I (1983) Effect of forced locomotor on the rest activity cycle of the cockroach. Behav Brain Res 8:351–360

    Article  PubMed  CAS  Google Scholar 

  46. von Buttel-Reepen HB (1900) Sind die bienen reflexmaschinen? Arthur Georgi, Leipzig

    Google Scholar 

  47. von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge

    Google Scholar 

  48. Yerushalmi S, Bodenhaimer S, Bloch G (2006) Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees. J Exp Biol 209:1044–1051

    Article  PubMed  Google Scholar 

  49. Zavodska R, Sauman I, Sehnal F (2003) Distribution of PER protein, pigment-dispersing hormone, prothoracicotropic hormone, and eclosion hormone in the cephalic nervous system of insects. J Biol Rhythm 18:106–122

    Article  CAS  Google Scholar 

  50. Zhu HS, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol 6:138–155

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guy Bloch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Eban-Rothschild, A., Bloch, G. (2012). Circadian Rhythms and Sleep in Honey Bees. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_3

Download citation

Publish with us

Policies and ethics