Journal of Insect Behavior

, Volume 32, Issue 3, pp 218–224 | Cite as

Suppression of Flight Activity by a Dopamine Receptor Antagonist in Honey Bee (Apis mellifera) Virgin Queens and Workers

  • Sayed Ibrahim FarkharyEmail author
  • Ken Sasaki
  • Shinya Hayashi
  • Ken-ichi Harano
  • Satoshi Koyama
  • Toshiyuki Satoh


Dopamine (DA), one of the biogenic amines, has been suggested to regulate the motor activities of various animals. In honey bees, it has been reported to promote locomotor activity in queens, workers, and males, and to regulate the flight activity of workers and males. The role of DA in the flight activity of queens, however, has not yet been investigated. In this study, we tested the roles of DA in the flight activity of virgin queens. We first injected the DA receptor antagonist flupenthixol (10−2 M or 10−3 M) into the abdomens of 6-day-old virgin queens and measured the time to flight initiation. The same experiment was performed in workers, to confirm previous findings and compare them to the virgin queens. We then injected 10−2 M flupenthixol into the queens and quantified their flight activity using a flight mill. The workers were deemed unsuitable for this round of experimentation. In both queens and workers, flupenthixol injection significantly delayed flight initiation. In flight mill experiments, flupenthixol decreased the flight performance of the queens in terms of distance, duration, and velocity. These results suggest the involvement of DA in the flight activity of virgin queens and workers, and indicate that DA is a key neuroactive substance in motor system activation with conserved effects among honey bee queens, workers, and males.


Dopamine flight activity flight initiation flight mill flupenthixol virgin queen worker bee 



We gratefully thank Dr. Yuya Fukano for assistance with statistical analysis and all members of the Laboratory of Ethology at Tokyo University of Agriculture and Technology for support and fruitful discussions. This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (grant numbers 26440181 and 17 K07491 to KS).


  1. Akasaka S, Sasaki K, Harano K, Nagao T (2010) Dopamine enhances locomotor activity for mating in male honeybees (Apis mellifera L). J Insect Physiol 56:1160–1166CrossRefGoogle Scholar
  2. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  3. Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc Natl Acad Sci U S A 104:2460–2464CrossRefGoogle Scholar
  4. Beggs KT, Tyndall JD, Mercer AR (2011) Honey bee dopamine and octopamine receptors linked to intracellular calcium signaling have a close phylogenetic and pharmacological relationship. PLoS One. CrossRefGoogle Scholar
  5. Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: Lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13–38CrossRefGoogle Scholar
  6. Buhl E, Schildberger K, Stevenson PA (2008) A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J Exp Biol 211:2346–2357CrossRefGoogle Scholar
  7. Carlson NR (2013) Physiology of behavior, 11th edn. Pearson, BostonGoogle Scholar
  8. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7:1096–1103CrossRefGoogle Scholar
  9. Claassen DE, Kammer AE (1986) Effects of octopamine, dopamine, and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. Dev Neurobiol 17:1–14CrossRefGoogle Scholar
  10. Cooper RL, Neckameyer WS (1999) Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B 122:199–210CrossRefGoogle Scholar
  11. Dasari S, Cooper RL (2004) Modulation of sensory-CNS-motor circuits by seroto- nin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227CrossRefGoogle Scholar
  12. Dickinson MH, Lehmann FO, Chan WP (1998) The control of mechanical power in insect flight. Am Zool 38:718–728CrossRefGoogle Scholar
  13. Dominguez JM, Hull EM (2005) Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86:356–368CrossRefGoogle Scholar
  14. Draper I, Kurshan PT, McBride E, Jackson FR, Kopin AS (2007) Locomotor activity is regulated by D2-like receptors in Drosophila: an anatomic and functional analysis. Dev Neurobiol 67:378–393CrossRefGoogle Scholar
  15. Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473CrossRefGoogle Scholar
  16. Farkhary SI, Sasaki K, Hayashi S, Harano KI, Koyama S, Satoh T (2017) Fighting and stinging responses are affected by a dopamine receptor blocker flupenthixol in honey bee virgin queens. J Insect Behav 30:717–727CrossRefGoogle Scholar
  17. Gilley DC, Tarpy DR (2005) Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474CrossRefGoogle Scholar
  18. Gole JWD, Orr GL, Downer RGH (1987) Pharmacology of octopamine, dopamine, and 5-hydroxytrptamine-stimulated cyclic AMP accumulation in the corpus cardiacum of the american cockroach, Periplaneta americana L. Arch Insect Biochem Physiol 5:119–128CrossRefGoogle Scholar
  19. Gmeinbauer R, Crailsheim K (1993) Glucose utilization during flight of honeybee (Apis mellifera) workers, drones and queens. J Insect Physiol 39:959–967CrossRefGoogle Scholar
  20. Harano K, Sasaki K, Nagao T (2005) Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens. Naturwissenschaften 92:310–313CrossRefGoogle Scholar
  21. Harano K, Sasaki M, Nagao T, Sasaki K (2008) Dopamine influences locomotor activity in honeybee queens: implications for a behavioural change after mating. Physiol Entomol 33:395–399CrossRefGoogle Scholar
  22. Harano K, Sasaki M, Sasaki K (2007) Effects of reproductive state on rhythmicity, locomotor activity and body weight in European honeybee, Apis mellifera (Hymenoptera, Apini) queens. Sociobiology 50:189–200Google Scholar
  23. Harris JW, Woodring J (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain. J Insect Physiol 38:29–35CrossRefGoogle Scholar
  24. Kramer PF, Christensen CH, Hazelwood LA et al (2011) Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J Neurosci 31:126–132CrossRefGoogle Scholar
  25. Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas Press, CheshireGoogle Scholar
  26. Lehmann FO, Bartussek J (2017) Neural control and precision of flight muscle activation in Drosophila. J Comp Physiol A 203:1–14CrossRefGoogle Scholar
  27. Lima SQ, Miesenböck G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–152CrossRefGoogle Scholar
  28. Mezawa R, Akasaka S, Nagao T, Sasaki K (2013) Neuroendocrine mechanisms underlying regulation of mating flight behaviors in male honey bees (Apis mellifera L.). Gen Comp Endocrinol 186:108–115CrossRefGoogle Scholar
  29. Mustard JA, Pham PM, Smith BH (2010) Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J Insect Physiol 56:422–430CrossRefGoogle Scholar
  30. Puhl JG, Mesce KA (2008) Dopamine activates the motor pattern for crawling in the medicinal leech. J Neurosci 28:4192–4200CrossRefGoogle Scholar
  31. Rhodes JS, Gammie SC, Garland T (2005) Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 45:438–455CrossRefGoogle Scholar
  32. Sasaki K, Nagao T (2013) Juvenile hormone-dopamine systems for the promotion of flight activity in males of the large carpenter bee Xylocopa appendiculata. Naturwissenschaften 100:1183–1186CrossRefGoogle Scholar
  33. Svensson E, Grillner S, Parker D (2001) Gating and braking of short- and long- term modulatory effects by interactions between colocalized neuromodulators. J Neurosci 21:5984–5992CrossRefGoogle Scholar
  34. Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15:37–46CrossRefGoogle Scholar
  35. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479CrossRefGoogle Scholar
  36. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sayed Ibrahim Farkhary
    • 1
    • 2
    • 3
    Email author
  • Ken Sasaki
    • 4
  • Shinya Hayashi
    • 2
  • Ken-ichi Harano
    • 4
  • Satoshi Koyama
    • 2
  • Toshiyuki Satoh
    • 2
  1. 1.Applied Veterinary Sciences, The United Graduate School of Veterinary SciencesGifu UniversityGifuJapan
  2. 2.Institute of AgricultureTokyo University of Agriculture and TechnologyTokyoJapan
  3. 3.Laboratory of Animal Husbandry and Management, Department of Animal Production, Faculty of Veterinary ScienceKabul UniversityKabulAfghanistan
  4. 4.Honey bee Science Research CenterTamagawa UniversityTokyoJapan

Personalised recommendations