Skip to main content
Log in

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

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akasaka S, Sasaki K, Harano K, Nagao T (2010) Dopamine enhances locomotor activity for mating in male honeybees (Apis mellifera L). J Insect Physiol 56:1160–1166

    Article  CAS  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • 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 104:2460–2464

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0026809

    Article  CAS  Google Scholar 

  • 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 48:13–38

    Article  CAS  Google Scholar 

  • Buhl E, Schildberger K, Stevenson PA (2008) A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J Exp Biol 211:2346–2357

    Article  CAS  Google Scholar 

  • Carlson NR (2013) Physiology of behavior, 11th edn. Pearson, Boston

    Google Scholar 

  • Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7:1096–1103

    Article  CAS  Google Scholar 

  • 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 17:1–14

    Article  CAS  Google Scholar 

  • Cooper RL, Neckameyer WS (1999) Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B 122:199–210

    Article  CAS  Google Scholar 

  • Dasari S, Cooper RL (2004) Modulation of sensory-CNS-motor circuits by seroto- nin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227

    Article  CAS  Google Scholar 

  • Dickinson MH, Lehmann FO, Chan WP (1998) The control of mechanical power in insect flight. Am Zool 38:718–728

    Article  CAS  Google Scholar 

  • Dominguez JM, Hull EM (2005) Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86:356–368

    Article  CAS  Google Scholar 

  • 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 67:378–393

    Article  CAS  Google Scholar 

  • Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

    Article  CAS  Google Scholar 

  • 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 30:717–727

    Article  Google Scholar 

  • Gilley DC, Tarpy DR (2005) Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474

    Article  Google Scholar 

  • 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 5:119–128

    Article  CAS  Google Scholar 

  • Gmeinbauer R, Crailsheim K (1993) Glucose utilization during flight of honeybee (Apis mellifera) workers, drones and queens. J Insect Physiol 39:959–967

    Article  CAS  Google Scholar 

  • Harano K, Sasaki K, Nagao T (2005) Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens. Naturwissenschaften 92:310–313

    Article  CAS  Google Scholar 

  • 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 33:395–399

    Article  Google Scholar 

  • 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 50:189–200

    Google Scholar 

  • 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 38:29–35

    Article  CAS  Google Scholar 

  • Kramer PF, Christensen CH, Hazelwood LA et al (2011) Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J Neurosci 31:126–132

    Article  CAS  Google Scholar 

  • Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas Press, Cheshire

    Google Scholar 

  • Lehmann FO, Bartussek J (2017) Neural control and precision of flight muscle activation in Drosophila. J Comp Physiol A 203:1–14

    Article  CAS  Google Scholar 

  • Lima SQ, Miesenböck G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–152

    Article  CAS  Google Scholar 

  • 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 186:108–115

    Article  CAS  Google Scholar 

  • 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 56:422–430

    Article  CAS  Google Scholar 

  • Puhl JG, Mesce KA (2008) Dopamine activates the motor pattern for crawling in the medicinal leech. J Neurosci 28:4192–4200

    Article  CAS  Google Scholar 

  • Rhodes JS, Gammie SC, Garland T (2005) Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 45:438–455

    Article  Google Scholar 

  • 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 100:1183–1186

    Article  CAS  Google Scholar 

  • Svensson E, Grillner S, Parker D (2001) Gating and braking of short- and long- term modulatory effects by interactions between colocalized neuromodulators. J Neurosci 21:5984–5992

    Article  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15:37–46

    Article  CAS  Google Scholar 

  • Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479

    Article  CAS  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sayed Ibrahim Farkhary.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farkhary, S.I., Sasaki, K., Hayashi, S. et al. Suppression of Flight Activity by a Dopamine Receptor Antagonist in Honey Bee (Apis mellifera) Virgin Queens and Workers. J Insect Behav 32, 218–224 (2019). https://doi.org/10.1007/s10905-019-09728-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-019-09728-7

Keywords

Navigation