Skip to main content

Appetite is correlated with octopamine and hemolymph sugar levels in forager honeybees

Abstract

Insects have rapidly changing energy demands, so they primarily rely on hemolymph and other carbohydrates to carry out life activities. However, how gustatory responsiveness and hemolymph sugar levels coordinate with one another to maintain energetic homeostasis in insects remains largely unknown for the highly social honeybee that goes through large physiological and behavioral changes. The potential role of biogenic amines and neuropeptides in the connection between the regulation of appetite and fluctuating sugar levels in the hemolymph, due to starvation, as the bee ages, was investigated. The largest appetite increase due to the starvation treatment was within the forager age class and this corresponded with an increase in octopamine levels in the brain along with a decline in hemolymph sugar levels. Adipokinetic hormone (AKH) was found in very small quantities in the brain and there were no significant changes in response to starvation treatment. Our findings suggest that the particularly dynamic levels of hemolymph sugar levels may serve as a monitor of the forager honeybee energetic state. Therefore, there may be a pathway in forager bees via octopamine responsible for their precise precipitous regulation of appetite, but to determine cause and effect relationships further investigation is needed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

AKH:

Adipokinetic hormone

GC–MS:

Gas chromatography–mass spectrometry

GLM:

Generalized linear model

GRS:

Gustatory response score

HPLC:

High-performance liquid chromatography

MANOVA:

Multivariate analysis of variance

PER assay:

Proboscis extension response assay

References

  1. Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223:451–464

    Article  CAS  PubMed  Google Scholar 

  2. Amdam GV, Norberg K, Page RE Jr, Erber J, Scheiner R (2006) Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behav Brain Res 169:201–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Behrends A, Scheiner R, Baker N, Amdam GV (2007) Cognitive aging is linked to social role in honey bees (Apis mellifera). Exp Gerontol 42(12):1146–1153

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119

    Article  CAS  Google Scholar 

  5. Blatt J, Roces F (2001) Haemolymph sugar levels in foraging honeybees (Apis mellifera carnica): dependence on metabolic rate and in vivo measurement of maximal rates of trehalose synthesis. J Exp Biol 204:2709–2716

    CAS  PubMed  Google Scholar 

  6. Blatt J, Roces F (2002) The control of proventriculus in the honeybee (Apis mellifera carnica L.) I. A dynamic process influenced by food quality and quantity? J Insect Physiol 48:643–654

    Article  CAS  PubMed  Google Scholar 

  7. Bounias M (1987) Propranolol and somatostatin interactions with the hyperglycemic effects of glucagon, octopamine, noradrenaline and cAMP in worker honeybees in vivo. Biochimie 69(6–7):655–660

    Article  CAS  PubMed  Google Scholar 

  8. Bounias M, Kruk I (1983) Adrenochrome as competitive inhibitor of epinephrine effects: a comparative study on trehalose and glucose levels in the honey-bee hemolymph. Comp Biochem Physiol C 74(1):143–150. https://doi.org/10.1016/0742-8413(83)90166-4

    Article  Google Scholar 

  9. Brockmann A, Annangudi SP, Richmond TA, Ament SA, Xie F, Southey BR, Rodriguez-Zas SR, Robinson GE, Sweedler JV (2009) Quantitative peptidomics reveal brain peptide signatures of behavior. Proc Natl Acad Sci 106(7):2383–2388. https://doi.org/10.1073/pnas.0813021106

    Article  PubMed  Google Scholar 

  10. Candy DJ (1978) Regulation of locust flight-muscle metabolism by octopamine and other compounds. Insect Biochem 8(3):177–181. https://doi.org/10.1016/0020-1790(78)90070-7

    Article  CAS  Google Scholar 

  11. Chan Q, Mutti NS, Foster LJ, Kocher SD, Amdam GV, Wolschin F (2011) The worker honeybee fat body proteome is extensively remodeled preceding a major life-history transition. PLoS One 6(9):e24794. https://doi.org/10.1371/journal.pone.0024794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cohen RW, Friedman S, Waldbauer GP (1988) Physiological control of nutrient self-selection in Heliothis zea larvae: the role of serotonin. J Insect Physiol 34(10):935–940. https://doi.org/10.1016/0022-1910(88)90129-1

    Article  CAS  Google Scholar 

  13. Cohen R, Mahoney D, Can H (2002) Possible regulation of feeding behavior in cockroach nymphs by the neurotransmitter octopamine. J Insect Behav 15(1):37–50

    Article  Google Scholar 

  14. Crailsheim K (1988) Intestinal transport of sugars in the honeybee (Apis mellifera L.). J Insect Physiol 34:839–845

    Article  CAS  Google Scholar 

  15. Davenport AP, Evans PD (1984) Changes in hemolymph octopamine levels associated with food-deprivation in the locust Schistocerca-gregaria. Physiol Entomol 9(3):269–274

    Article  CAS  Google Scholar 

  16. Evans JD, Schwarz RS, Chen YP, Budge G, Cornman RS, Rua P, Miranda J, Foret S, Foster L, Gauthier L, Genersch E, Gisder S, Jarosch A, Kucharski R, Lopez D, Lun CM, Moritz RFA, Maleszka R, Muñoz I, Pinto MA (2013) Coloss beebook volume I: standard methods for Apis mellifera research, 1st edn. Ibra Publications, Bristol, p 636

    Google Scholar 

  17. Fell RD (1990) The qualitative and quantitative analysis of insect hemolymph sugars by high-performance thin-layer chromatography. Comp Biochem Physiol 95(4):539–544

    Article  Google Scholar 

  18. Fields PE, Woodring JP (1991) Octopamine mobilization of lipids and carbohydrates in the house cricket, Acheta domesticus. J Insect Physiol 37(3):193–199. https://doi.org/10.1016/0022-1910(91)90069-C

    Article  CAS  Google Scholar 

  19. Friedman S, Waldbauer GP, Eertmoed JE, Naeem M, Ghent AW (1991) Blood trehalose levels have a role in the control of dietary self-selection by Heliothis zea larvae. J Insect Physiol 37(12):919–928. https://doi.org/10.1016/0022-1910(91)90007-m

    Article  CAS  Google Scholar 

  20. Fryer JH, Moore NS, Williams HH, Young CM (1955) A study of the interrelationship of the energy-yielding nutrients, blood glucose levels, and subjective appetite in man. J Lab Clin Med 45(5):684–696

    CAS  PubMed  Google Scholar 

  21. 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(1):29–35

    Article  CAS  Google Scholar 

  22. Harrison JM (1986) Caste-specific changes in honeybee flight capacity. Physiol Zool 59(2):175–187

    Article  Google Scholar 

  23. Ishida Y, Ozaki M (2011) A putative octopamine/tyramine receptor mediating appetite in a hungry fly. Naturwissenschaften 98(7):635–638. https://doi.org/10.1007/s00114-011-0806-z

    Article  CAS  PubMed  Google Scholar 

  24. Jaycox ER, Skowrone W, Guynn G (1974) Behavioral-changes in worker honey bees (Apis mellifera) induced by injections of a juvenile hormone mimic. Ann Entomol Soc Am 67(4):529–535

    Article  Google Scholar 

  25. Klowden M (2013) Physiological systems in insects, 3rd edn. Academic Press, New York, p 677

    Google Scholar 

  26. Kodrík D (2008) Adipokinetic hormone functions that are not associated with insect flight. Physiol Entomol 33(3):171–180. https://doi.org/10.1111/j.1365-3032.2008.00625.x

    Article  CAS  Google Scholar 

  27. Konuma T, Morooka N, Nagasawa H, Nagata S (2012) Knockdown of the adipokinetic hormone receptor increases feeding frequency in the two-spotted cricket Gryllus bimaculatus. Endocrinology 153(7):3111–3122

    Article  CAS  PubMed  Google Scholar 

  28. Koon AC, Ashley J, Barria R, DasGupta S, Brain R, Waddell S, Alkema MJ, Budnik V (2011) Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat Neurosci 14(2):190–199. https://doi.org/10.1038/nn.2716

    Article  CAS  PubMed  Google Scholar 

  29. Lange AB (2009) Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162(1):18–26. https://doi.org/10.1016/j.ygcen.2008.05.021

    Article  CAS  PubMed  Google Scholar 

  30. Lee GH, Park JH (2004) Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167(1):311–323. https://doi.org/10.1534/genetics.167.1.311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Leibowitz S, Stanley B (1986) Neurochemical controls of appetite. In: Rolls E (ed) Feeding behavior: neural and humoral controls. Academic Press, New York, pp 191–234

    Chapter  Google Scholar 

  32. Linn CE, Roelofs WL (1993) Levels of biogenic amines and peptides in individual corn earworm moths, Helicoverpa zea, using high performance liquid chromatography with electrochemical detection. Insect Biochem Mol Biol 23(3):367–373. https://doi.org/10.1016/0965-1748(93)90020-S

    Article  CAS  PubMed  Google Scholar 

  33. Long TF, Murdock LL (1983) Stimulation of blowfly feeding-behavior by octopaminergic drugs. Proc Natl Acad Sci Biol 80(13):4159–4163. https://doi.org/10.1073/pnas.80.13.4159

    Article  CAS  Google Scholar 

  34. Lorenz MW, Kellner R, Woodring J, Hoffmann KH, Gade G (1999) Hypertrehalosaemic peptides in the honeybee (Apis mellifera): purification, identification and function. J Insect Physiol 45(7):647–653

    Article  CAS  PubMed  Google Scholar 

  35. Lorenz MW, Kellner R, Völkl W, Hoffmann KH, Woodring J (2001) A comparative study on hypertrehalosaemic hormones in the Hymenoptera: sequence determination, physiological actions and biological significance. J Insect Physiol 47(6):563–571

    Article  CAS  PubMed  Google Scholar 

  36. Mayack C, Naug D (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J Insect Physiol 56(11):1572–1575

    Article  CAS  PubMed  Google Scholar 

  37. Mayack C, Naug D (2011) A changing but not an absolute energy budget dictates risk-sensitive behaviour in the honeybee. Anim Behav 82(3):595–600

    Article  Google Scholar 

  38. Mayack C, Naug D (2013) Individual energetic state can prevail over social regulation of foraging in honeybees. Behav Ecol Sociobiol 67(6):929–936. https://doi.org/10.1007/s00265-013-1517-6

    Article  Google Scholar 

  39. Medeiros PM, Simoneit BRT (2007) Gas chromatography coupled to mass spectrometry for analyses of organic compounds and biomarkers as tracers for geological, environmental, and forensic research. J Sep Sci 30(10):1516–1536. https://doi.org/10.1002/jssc.200600399

    Article  CAS  PubMed  Google Scholar 

  40. Nisimura T, Seto A, Nakamura K, Miyama M, Nagao T, Tamotsu S, Yamaoka R, Ozaki M (2005) Experiential effects of appetitive and nonappetitive odors on feeding behavior in the blowfly, Phormia regina: a putative role for tyramine in appetite regulation. J Neurosci 25:7507–7516

    Article  CAS  PubMed  Google Scholar 

  41. Pankiw T, Page RE Jr (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 185:207–213

    Article  CAS  PubMed  Google Scholar 

  42. Pankiw T, Page RE Jr (2000) Response thresholds to sucrose predict foraging division of labor in honeybees. Behav Ecol Sociobiol 47:265–267

    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

    Article  Google Scholar 

  44. Robinson GE (1985) Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. J Insect Physiol 31:277–282

    Article  CAS  Google Scholar 

  45. Robinson GE (1987) Regulation of honey bee age polyethism by juvenile hormone. Behav Ecol Sociobiol 20:329–338

    Article  Google Scholar 

  46. Roeder T, Seifert M, Kahler C, Gewecke M (2003) Tyramine and octopamine: antagonistic modulators of behavior and metabolism. Arch Insect Biochem Physiol 54(1):1–13. https://doi.org/10.1002/arch.10102

    Article  PubMed  Google Scholar 

  47. Scheiner R (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4:259–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136(2):545–553

    Article  CAS  PubMed  Google Scholar 

  49. Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142

    Article  Google Scholar 

  50. Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184(5):481–488. https://doi.org/10.1007/s003590050348

    Article  CAS  PubMed  Google Scholar 

  51. Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187(1):53–61

    Article  CAS  PubMed  Google Scholar 

  52. Schulz DJ, Barron AB, Robinson GE (2002a) A role for octopamine in honey bee division of labor. Brain Behav Evolut 60(6):350–359

    Article  Google Scholar 

  53. Schulz DJ, Sullivan JP, Robinson GE (2002b) Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm Behav 42(2):222–231. https://doi.org/10.1006/hbeh.2002.1806

    Article  CAS  Google Scholar 

  54. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293

    Article  Google Scholar 

  55. Simcock NK, Gray H, Bouchebti S, Wright GA (2018) Appetitive olfactory learning and memory in the honeybee depend on sugar reward identity. J Insect Physiol 106(Pt 1):71–77. https://doi.org/10.1016/j.jinsphys.2017.08.009

    Article  CAS  PubMed  Google Scholar 

  56. Simpson SJ, Raubenheimer D (1993) The central role of the haemolymph in the regulation of nutrient intake in insects. Physiol Entomol 18:395–403

    Article  CAS  Google Scholar 

  57. Thompson SN (2003) Trehalose—the insect ‘blood’ sugar. Adv Insect Physiol 31:205–285

    Article  CAS  Google Scholar 

  58. Toth AL, Robinson GE (2005) Worker nutrition and division of labour in honeybees. Anim Behav 69(2):427–435

    Article  Google Scholar 

  59. Toth AL, Kantarovich S, Meisel AF, Robinson GE (2005) Nutritional status influences socially regulated foraging ontogeny in honey bees. J Exp Biol 208:4641–4649

    Article  PubMed  Google Scholar 

  60. Van der Horst DJ (2003) Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp Biochem Physiol B 136(2):217–226. https://doi.org/10.1016/S1096-4959(03)00151-9

    Article  CAS  PubMed  Google Scholar 

  61. Veenstra JA, Rodriguez L, Weaver RJ (2012) Allatotropin, leucokinin and AKH in honey bees and other hymenoptera. Peptides 35(1):122–130

    Article  CAS  PubMed  Google Scholar 

  62. Wada-Katsumata A, Yamaoka R, Aonuma H (2011) Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica. J Exp Biol 214(10):1707–1713. https://doi.org/10.1242/jeb.051565

    Article  CAS  PubMed  Google Scholar 

  63. 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(5):471–479. https://doi.org/10.1007/s003590050347

    Article  CAS  PubMed  Google Scholar 

  64. Wang Y, Brent CS, Fennern E, Amdam GV (2012) Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 8(6):e1002779. https://doi.org/10.1371/journal.pgen.1002779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Woodring J, Boulden M, Das S, Gäde G (1993) Studies on blood sugar homeostasis in the honeybee (Apis mellifera, L.). J Insect Physiol 39(1):89–97

    Article  CAS  Google Scholar 

  66. Woodring J, Das S, Gäde G (1994) Hypertrehalosemic factors from the corpora cardiaca of the honeybee (Apis mellifera) and the paper wasp (Polistes exclamans). J Insect Physiol 40(8):685–692

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mariann Pü, Brian Shields, Rebecca Zhou, Victor Le, and Elizabeth Eppley for assistance with hemolymph extractions, brain dissections, and data collection. The authors would also like to thank Dr. Kathleen Howard for providing access to her lyophilizer and assisting with its use. This work was supported by an Alexander von Humboldt Foundation Fellowship award to CM, a Swarthmore College Surdna Summer Research Fellowship to KC, and a Howard Hughes Medical Institute Fellowship to NP.

Data availability

The datasets generated during the current study are available in the Open Science Framework repository, https://osf.io/h4c6e/.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christopher Mayack.

Ethics declarations

Ethical approval

All honeybees were handled humanely in accordance with current ethical standards. Special ethical approval is not required to carry out this study.

Conflict of interest

The authors declare that there are no competing interests.

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

Verify currency and authenticity via CrossMark

Cite this article

Mayack, C., Phalen, N., Carmichael, K. et al. Appetite is correlated with octopamine and hemolymph sugar levels in forager honeybees. J Comp Physiol A 205, 609–617 (2019). https://doi.org/10.1007/s00359-019-01352-2

Download citation

Keywords

  • Starvation
  • Aging
  • Biogenic amines
  • Trehalose
  • Hemolymph