Journal of Comparative Physiology A

, Volume 193, Issue 2, pp 167–180 | Cite as

Manipulating the light/dark cycle: effects on dopamine levels in optic lobes of the honey bee (Apis mellifera) brain

  • Elizabeth Carrington
  • Ilona C. Kokay
  • Jane Duthie
  • Robert Lewis
  • Alison R. Mercer
Original Paper


This study examines the relationship between cyclical variations in optic-lobe dopamine levels and the circadian behavioural rhythmicity exhibited by forager bees. Our results show that changing the light–dark regimen to which bees are exposed has a significant impact not only on forager behaviour, but also on the levels of dopamine that can be detected in the optic lobes of the brain. Consistent with earlier reports, we show that foraging behaviour exhibits properties characteristic of a circadian rhythm. Foraging activity is entrained by daily light cycles to periods close to 24 h, it changes predictably in response to phase shifts in light, and it is able to free-run under constant conditions. Dopamine levels in the optic lobes also undergo cyclical variations, and fluctuations in endogenous dopamine levels are influenced significantly by alterations to the light/dark cycle. However, the time course of these changes is markedly different from changes observed at a behavioural level. No direct correlation could be identified between levels of dopamine in the optic lobes and circadian rhythmic activity of the honey bee.


Circadian rhythms Insect visual system Biogenic amines 



We gratefully acknowledge and thank Ken Miller for assistance with the illustrations, and Kim Garrett for maintaining the honey bee colonies. This work was funded by the University of Otago (UORG 200100620). The experiments described in this work comply with the “Principles of Animal Care” publication No. 86–23 of the National Institute of Health, and also laws of New Zealand regulating scientific research.


  1. Andretic R, Hirsh J (2000) Circadian modulation of dopamine receptor responsiveness in Drosophila melanogaster. Proc Natl Acad Sci USA 97:1873–1878PubMedCrossRefGoogle Scholar
  2. Beggs KT, Hamilton IS, Kurshan PT, Mustard JA, Mercer AR (2005) Characterization of a D2-like dopamine receptor (AmDOP3) in honey bee, Apis mellifera. Insect Biochem Mol Biol 35:873–882PubMedCrossRefGoogle Scholar
  3. Ben-Shahar Y, Leung H-T, Pak WL, Sokolowski MB, Robinson GE (2003) cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J Exp Biol 206:2507–2515PubMedCrossRefGoogle Scholar
  4. Blenau W, Erber J, Baumann A (1998) Characterization of a dopamine D1 receptor from Apis mellifera-cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70:15–23PubMedCrossRefGoogle Scholar
  5. Bloch G, Toma DP, Robinson GE (2001) Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J Biol Rhythms 16:444–456PubMedCrossRefGoogle Scholar
  6. 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 464:269–284PubMedCrossRefGoogle Scholar
  7. Colwell CS, Page TL (1990) A circadian rhythm in neural activity can be recorded from the central nervous system of the cockroach. J Comp Physiol 166:643–649CrossRefGoogle Scholar
  8. Crailsheim K, Hrassnigg N, Stabentheiner A (1996) Diurnal behavioural differences in forager and nurse honey bees (Apis mellifera carnica Pollm). Apidologie 27:235–244CrossRefGoogle Scholar
  9. Cymborowski B, King V (1996) Circadian regulation of Fos-like expression in the brain of the blow fly Calliphora vicina. Comp Biochem Physiol 115:239–246Google Scholar
  10. Cymborowski B, Lewis RD, Hong SF, Saunders DS (1994) Circadian locomotor activity-rhythms and their entrainment to light–dark cycles continue in flies (Calliphora vicina) surgically deprived of their optic lobes. J Insect Physiol 40:501–510CrossRefGoogle Scholar
  11. Dowling JE (1991) Retinal neuromodulation: the role of dopamine. Vis Neurosci 7:87–97PubMedGoogle Scholar
  12. Edwards A (1980) Cholinesterase activity in the cockroach central nervous system. Insect Biochem 10:387–392CrossRefGoogle Scholar
  13. Enright JT (1965) The search for rhythmicity in biological time series. J Theoret Biol 8:226–268Google Scholar
  14. Eskin A, Corrent G, Lin C-Y, McAdoo DJ (1982) Mechanism for shifting the phase of a circadian rhythm by serotonin: Involvement of cAMP. Proc Natl Acad Sci USA 79:660–664PubMedCrossRefGoogle Scholar
  15. Ewer J, Frisch B, Hamblen-Coyle MJ, Rasbash M, Hall JC (1992) Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells’ influence on circadian behavioral rhythms. J Neurosci 12:3321–3349PubMedGoogle Scholar
  16. von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  17. Frisch B, Aschoff J (1987) Circadian rhythms in honeybees: entrainment by feeding cycles. Physiol Entomol 12:41–49Google Scholar
  18. Frisch B, Koeniger N (1994) Social synchronization of the activity rhythms of honeybees within a colony. Behav Ecol Sociobiol 35:91–98CrossRefGoogle Scholar
  19. Frisch B, Hardin PE, Hamblen-Coyle MJ, Rosbash M, Hall JC (1994) A promotorless period gene mediates behavioural rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12:555–570PubMedCrossRefGoogle Scholar
  20. Germ M, Kral K (1995) Influence of visual deprivation on levels of dopamine and serotonin in the visual system of house crickets, Acheta domesticus. J Insect Physiol 41:57–63CrossRefGoogle Scholar
  21. Helfrich-Förster C, Homberg U (1993) Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177–190PubMedCrossRefGoogle Scholar
  22. Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594PubMedCrossRefGoogle Scholar
  23. Homberg U, Reischig T, Stengl M (2003) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591PubMedCrossRefGoogle Scholar
  24. Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266:343–357CrossRefGoogle Scholar
  25. Humphries MA, Mustard JA, Hunter SJ, Mercer AR, Ward V, Ebert PR. 2003. Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in mushroom bodies of the honeybee brain. J Neurobiol 55:315–330PubMedCrossRefGoogle Scholar
  26. Kaiser W (1988) Busy bees need rest too: behavioral and electromyographic sleep signs in honeybees. J Comp Physiol A 163:565–584CrossRefGoogle Scholar
  27. Kaiser W, Steiner-Kaiser J (1983) Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301:707–709PubMedCrossRefGoogle Scholar
  28. Kokay IC, Mercer AR (1996) Characterisation of dopamine receptors in insect (Apis mellifera) brain. Brain Res 706:47–56PubMedCrossRefGoogle Scholar
  29. Kokay IC, Mercer AR (1997) Age-related changes in dopamine receptor densities in the brain of the honey bee, Apis mellifera. J Comp Physiol 181:415–423CrossRefGoogle Scholar
  30. Kokay IC, McEwan J, Mercer AR (1998) Autoradiographic localisation of [3H]-SCH23390 and [3H]-spiperone binding sites in honey bee brain. J Comp Neurol 394:29–37PubMedCrossRefGoogle Scholar
  31. Kurshan PT, Hamilton IS, Mustard JA, Mercer AR (2003) Developmental changes in expression patterns of two dopamine receptor genes in mushroom bodies of the honeybee, Apis mellifera. J Comp Neurol 466:91–103PubMedCrossRefGoogle Scholar
  32. Lindauer M (1961) Communication among social bees. Harvard University Press, Cambridge, pp 143Google Scholar
  33. Linn CE, Campbell MG, Poole KR, Roelofs WL (1994) Studies on biogenic amines and their metabolites in nervous tissue and hemolymph of adult male cabbage looper moths: I. Quantitation of photoperiod changes. Comp Biochem Physiol C 108:73–85CrossRefGoogle Scholar
  34. Meinertzhagen IA, Pyza E (1996) Daily rhythms in cells of the fly’s optic lobe: taking time out from the circadian clock. Trends Neurosci 19:285–291PubMedCrossRefGoogle Scholar
  35. Meinertzhagen IA, Pyza E (1999) Neurotransmitter regulation of circadian structural changes in the fly’s visual system. Microsc Res Tech 45:96–105PubMedCrossRefGoogle Scholar
  36. Mobbs PG (1982) The brain of the honey bee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298:309–354CrossRefGoogle Scholar
  37. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857CrossRefGoogle Scholar
  38. Moore D, Rankin MA (1985) Circadian locomotor rhythms in individual honey bees. Physiol Entomol 10:191–197Google Scholar
  39. Moore D, Rankin MA (1993) Light and temperature entrainment of a locomotor rhythm in honeybees. Physiol Entomol 18:271–278Google Scholar
  40. Moore D, Seigfried D, Wilson R, Rankin MA (1989) The influence of time of day on the foraging behaviour of the honeybee, Apis mellifera L. J Biol Rhythms 4:305–325PubMedCrossRefGoogle Scholar
  41. Moore D, Angel JE, Cheesman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160CrossRefGoogle Scholar
  42. Muszynska-Pytel M, Cymborowski B (1978a) The role of serotonin in regulation of circadian rhythms of locomotor activity in the cricket (Acheta domesticus L.). I. Circadian variations in serotonin concentrations in the brain and hemolymph. Comp Biochem Physiol 59C:13–15Google Scholar
  43. Muszynska-Pytel M, Cymborowski B (1978b) The role of serotonin in regulation of the circadian rhythms of locomotor activity in the cricket (Acheta domesticus L.). II. Distribution of serotonin and variations in different brain structure. Comp Biochem Physiol 59C:17–20Google Scholar
  44. Nishiitsutsuji-Uwo J, Pittendrigh CS (1968) Central nervous system control of circadian rhythmicity in the cockroach. II The optic lobes, locus of the driving oscillator? Z Physiol 58:14–46Google Scholar
  45. Owen MD, Pfaff L, Sloley BD (1987) The absence of diel change in the concentrations of dopamine, 5-hydroxytryptamine and their metabolites in the cerebral ganglia of the cockroach, Periplaneta americana. Insect Biochem 17:723–729CrossRefGoogle Scholar
  46. Page TL (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75PubMedCrossRefGoogle Scholar
  47. Page TL (1983) Regeneration of the optic tracts and circadian pacemaker activity in the cockroach Leucophaea maderae. J Comp Physiol 152:231–240CrossRefGoogle Scholar
  48. Page TL (1985) Clocks and circadian rhythms. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 6. Pergamon, New York, pp 577–652Google Scholar
  49. Page TL (1987) Serotonin phase-shifts the circadian rhythm of locomotor activity in the cockroach. J Biol Rhythms 2:23–34PubMedCrossRefGoogle Scholar
  50. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356PubMedCrossRefGoogle Scholar
  51. Prée J, Rutschke E (1983) Daily rhythm of the content of dopamine in the brain of the cockroach (Periplaneta americana L.). Zool Jb Physiol 87:455–460Google Scholar
  52. Proll MA, Morgan WW (1982) Adaptation of retinal dopamine neuron activity in light-adapted rats to darkness. Brain Res 241:359–361PubMedCrossRefGoogle Scholar
  53. Proll MA, Kamp CW, Morgan WW (1982) Use of liquid chromatography with electrochemistry to measure effects of varying intensities of white light on DOPA accumulation in rat retinas. Life Sci 30:11–19PubMedCrossRefGoogle Scholar
  54. Purnell MT, Mitchell CJ, Taylor DJ, Kokay IC, Mercer AR (2000) The influence of endogenous dopamine levels on the density of [3H]SCH23390-binding sites in the brain of the honey bee, Apis mellifera L. Brain Res 855:206–216PubMedCrossRefGoogle Scholar
  55. Reischig T, Stengl M (2003) Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae). J Exp Biol 206:1877–1886PubMedCrossRefGoogle Scholar
  56. Renn SCP, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioural circadian rhythms in Drosophila. Cell 99:791–802PubMedCrossRefGoogle Scholar
  57. Renner M (1960) The contribution of the honey bee to the study of time-sense and astronomical orientation. Cold Spring Harbor Symp Quant Biol XXV:361–367Google Scholar
  58. Sokolove PG (1975) Localization of the cockroach optic lobe circadian pacemaker with microlesions. Brain Res 87:13–21PubMedCrossRefGoogle Scholar
  59. Southwick EE, Moritz RFA (1987) Social synchronization of circadian rhythms of metabolism in honeybees (Apis mellifera). Physiol Entomol 12:209–212Google Scholar
  60. Spangler HG (1972) Daily activity rhythms of individual worker and drone honeybees. Ann Entomol Soc Am 65:1073–1076Google Scholar
  61. Spangler HG (1973) Role of light in altering the circadian oscillations of the honey bee. Ann Entomol Soc Am 66:449–451Google Scholar
  62. Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A 175:203–213PubMedCrossRefGoogle Scholar
  63. Stussi T (1972) Ontogenese du rythme circadian de la despense energetique chez l’abeille. Arch Sci Physiol (Paris) 26:161–173Google Scholar
  64. Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Natl Acad Sci USA 97:6914–6919PubMedCrossRefGoogle Scholar
  65. Tomioka K, Chiba Y (1989) Light cycle during post-embryonic development affects adult circadian parameters of the cricket (Gryllus bimaculatus) optic lobe pacemaker. J Insect Physiol 35:273–276CrossRefGoogle Scholar
  66. Tomioka K, Ikeda M, Nagao T, Tamotsu S (1993) Involvement of serotonin in the circadian rhythm of an insect visual system. Naturwiss 80:37–139CrossRefGoogle Scholar
  67. Williams JA, Naylor E (1978) A procedure for the assessment of significance of rhythmicity in time series data. Int J Chronobiol 5:435–444Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Elizabeth Carrington
    • 1
  • Ilona C. Kokay
    • 2
  • Jane Duthie
    • 1
  • Robert Lewis
    • 3
  • Alison R. Mercer
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Department of Anatomy and Structural BiologyUniversity of OtagoDunedinNew Zealand
  3. 3.Biological SciencesUniversity of AucklandAucklandNew Zealand

Personalised recommendations