Journal of Comparative Physiology A

, Volume 174, Issue 6, pp 731–739 | Cite as

Physiological correlates of division of labor among similarly aged honey bees

  • Z.-Y. Huang
  • G. E. Robinson1
  • D. W. Borst


Hormone analyses and exocrine gland measurements were made to probe for physiological correlates of division of labor among similarly aged adult worker honey bees (Apis mellifera L.). Middle-age bees (ca. 2 weeks old) performing different tasks showed significant differences in both juvenile hormone (JH) biosynthesis rates and hemolymph titers; guards and undertakers had high JH, and wax producers and food storers, low JH. Guards and undertakers had similar hormone levels to foragers, even though they were 10 days younger than foragers. No differences in JH were detected among young bees (1-week-old queen attendants and nurses) or older bees (3–4 week-old pollen foragers, non-pollen foragers, and soldiers). Hypopharyngeal gland size was inversely correlated with worker age and rate of JH biosynthesis, but soldiers had significantly larger hypopharyngeal glands than did foragers, despite their similar age and JH level. Results from soldiers indicate that exocrine gland development is not always linked with age-related behavior and endocrine development; they also support the recent claim that soldiers constitute a group of older bees that are distinct from foragers. Hormonal analyses indicate that the current model of JH's role in honey bee division of labor needs to be expanded because high levels of JH are associated with several other tasks besides foraging. JH may be involved in the regulation of division of labor among similarly aged workers in addition to its role in age-related division of labor.

Key words

Corpora allata Division of labor Hypopharyngeal glands Juvenile hormone Social insects 



Juvenile hormone




corpora allata


high performance liquid chromatography


thin layer chromatography


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  1. Breed MD (1983) Correlations between aggressiveness and corpora allata volume, social isolation, age and dietary protein in worker honeybees. Insectes Sociaux 30:482–495Google Scholar
  2. Breed MD, Robinson GE, Page RE (1990) Division of labor during honey bee colony defense. Behav Ecol Sociobiol 27:395–101Google Scholar
  3. Brouwers EVM (1982) Measurement of hypopharyngeal gland activity in the honeybee. J Apic Res 21:193–198Google Scholar
  4. Brouwers EVM (1983) Activation of the hypopharyngeal glands of honeybees in winter. J Apic Res 22:137–141Google Scholar
  5. Butler CG (1973) Perception of the queen by workers in the honeybee colony. J Apic Res 12:159–166Google Scholar
  6. Calderone NW, Page RE (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17–25Google Scholar
  7. Crailsheim K (1991) Interadult feeding of jelly in honeybee (Apismellifera L.) colonies. J Comp Physiol B 161:55–60Google Scholar
  8. Crailsheim K (1992) The flow of jelly within a honeybee colony. J Comp Physiol B 162:681–689Google Scholar
  9. Crailsheim K, Stolberg E (1989) Influence of diet, age and colony condition upon intestinal proteolytic activity and size of the hypopharyngeal glands in the honeybee (Apis mellifera L.). J Insect Physiol 35:595–602Google Scholar
  10. De Kort CAD, Koopmanschap AB, Strambi C, Strambi A (1985) The application and evaluation of a radioimmunoassay for measuring juvenile hormone titres in Colorado beetle haemolymph. Insect Biochem 15:771–775Google Scholar
  11. Denlinger DL, Shrukla M, Faustini DL (1984) Juvenile hormone involvement in pupal diapause of the flesh fly Sarcophaga crassipalpis: regulation of infradian cycles of O2 consumption. J Exp Biol 109:191–199Google Scholar
  12. Fergusson LA, Winston ML (1988) The influence of wax deprivation on temporal polyethism in honey bee (Apis mellifera L.) colonies. Can J Zool 66:1997–2001Google Scholar
  13. Fluri P, Lüscher M, Wille H, Gerig L (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees. J Insect Physiol 28:61–68Google Scholar
  14. Free JB, Ferguson AW, Simpkins JR (1992) The behaviour of queen honeybees and their attendants. Physiol Entomol 17:43–55Google Scholar
  15. Goodman WG, Coy DC, Baker FC, Xu L, Toong YC (1990) Development and application of a radioimmunoassay for the juvenile hormones. Insect Biochem 20:357–364Google Scholar
  16. Goodman WG, Huang Z-Y, Robinson GE, Strambi A, Strambi C (1993) A comparison of two juvenile hormone radioimmunoassays. Arch Insect Biochem Physiol 23:147–152Google Scholar
  17. Hagenguth H, Rembold H (1978) Identification of juvenile hormone 3 as the only juvenile hormone homolog in all developmental stages of the honey bee. Z Naturforsch 33C:847–850Google Scholar
  18. Harrison JM (1986) Caste-specific changes in honeybee flight capacity. Physiol Zool 59:175–187Google Scholar
  19. Hassanein MH (1952) The effects of infection with Nosema apis on the pharyngeal salivary glands of the worker honey-bee. Proc R Entomol Soc Lond A 27:22–27Google Scholar
  20. Haydak MH (1957) Changes with age in the appearance of some internal organs of the honeybee. Bee World 38:197–207Google Scholar
  21. Huang Z-Y (1990) A simple in vivo estimation of hypopharyngeal gland activity in honeybees (Apis mellifera). J Apic Res 29:75–81Google Scholar
  22. Huang Z-Y, Robinson GE (1992) Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sei USA 89:11726–11729Google Scholar
  23. Huang Z-Y, Otis GW, Teal PEA (1989) Nature of brood signal activating the protein synthesis of hypopharyngeal gland in honey bees, Apis mellifera (Apidae: Hymenoptera). Apidologie 20:455–164Google Scholar
  24. Huang Z-Y Robinson GE, Tobe SS, Yagi KJ, Strambi C, Strambi A, Stay B (1991) Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis. J Insect Physiol 37:733–741Google Scholar
  25. Hunnicutt, D, Toong YC, Borst DW (1989) A chiral specific antiserum for juvenile hormone. Am Zool 29:48aGoogle Scholar
  26. Jaycox ER (1976) Behavioral changes in worker honey bees (Apis mellifera L.) after injection with synthetic juvenile hormone (Hymenoptera: Apidae). J Kans Entomol Soc 49:165–170Google Scholar
  27. Jaycox ER, Skowronek W, Gwynn G (1974) Behavioral changes in worker honey bees (Apis mellifera) induced by injections of a juvenile hormone mimic. Ann Entomol Soc Am 67:529–534Google Scholar
  28. Jeanne RL (ed) (1987) Inter-individual behavioral variability in social insects. Westview Press, Boulder, ColoradoGoogle Scholar
  29. Kaatz H-H, Hagedorn HH, Engels W (1985) Culture of honeybee organs: development of a new medium and the importance of tracheation. In Vitro Cell Dev Biol 21:347–352Google Scholar
  30. King GE (1933) The larger glands in the worker honey-bee. A correlation of activity with age and with physiological functioning. Ph.D. Thesis, University of Illinois, Urbana, IllinoisGoogle Scholar
  31. Maurizio A (1954) Pollenernhrung und Lebensvorgänge bei der Honigbiene. Landw Jrb Schweiz 68:115–182Google Scholar
  32. Moore AJ, Breed MD, Moore MJ (1987) The guard honey bee: ontogeny and behavioural variability of workers performing a specialized task. Anim Behav 35:1159–1167Google Scholar
  33. Muller EJ, Hepburn HR (1992) Temporal and spatial patterns of wax secretion and related behavior in the division of labour of the honeybee (Apis mellifera capensis). J Comp Physiol A 171:111–115Google Scholar
  34. O'Donnell S, Jeanne RL (1993) Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis). Physiol Entomol 18:189–194Google Scholar
  35. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press Princeton, New JerseyGoogle Scholar
  36. Page RE, Robinson GE (1991) The genetics of division of labour in honey bee colonies. Adv Insect Physiol 23:117–171Google Scholar
  37. Pellet FC (1938) History of American beekeeping. Collegiate Press, Ames, IAGoogle Scholar
  38. Phillips EF (1915) Beekeeping. MacMillan, New YorkGoogle Scholar
  39. Pickard RS, Kither GY (1983) An evaluation of shaking and displacement methods for separating a sample of honeybees with large hypopharyngeal glands from the remainder of a colony. J Apic Res 22:101–106Google Scholar
  40. Pratt GE, Tobe SS (1974) Juvenile hormones radiobiosynthesized by corpora allata of adult female locusts in vitro. Life Sei 14:575–86Google Scholar
  41. Robinson GE (1985) Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. J Insect Physiol 31:277–282Google Scholar
  42. Robinson GE (1987a) Regulation of honey bee age polyethism by juvenile hormone. Behav Ecol Sociobiol 20:329–338Google Scholar
  43. Robinson GE (1987b) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J Comp Physiol A 160:613–619Google Scholar
  44. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665Google Scholar
  45. Robinson GE, Page RE (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358Google Scholar
  46. Robinson GE, Page RE (1989) Genetic determination of nectar foraging, pollen foraging, and nest-side scouting in honey bee colonies. Behav Ecol Sociobiol 24:317–323Google Scholar
  47. Robinson GE, Strambi A, Strambi C, Paulino-Simões ZL, Tozeto SO, Barbosa JMN (1987) Juvenile hormone titers in Africanized and European honey bees in Brazil. Gen Comp Endocrinol 66:457–459Google Scholar
  48. Robinson GE, Page RE., Strambi C, Strambi A (1989) Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246:109–112Google Scholar
  49. Robinson GE, Strambi C, Strambi A, Feldlaufer MF (1991) Comparison of juvenile hormone and ecdysteroid haemolymph titers in adult worker and queen honey bees (Apis mellifera). J Insect Physiol 37:929–935Google Scholar
  50. Rösch GA (1925) Untersuchungen über die Arbeitsteilung im Bienenstaat, I. Teil: Die Tätigkeiten im normalen Bienenstaate und ihre Beziehungen zum Alter der Arbeitsbienen. Z Vergl Physiol 2:571–631Google Scholar
  51. Rösch GA (1930) Untersuchungen über die Arbeitsteilung im Bienenstaat, II. Die Tätigkeiten der Arbeitsbienen unter experimentell veränderten Bedingungen. Z Vergl Physiol 12:1–71Google Scholar
  52. Rutz W, Gerig L, Wille H, Lüscher M (1974) A bioassay for juvenile hormone (JH) effects of insect growth regulators (IGR) on adult worker honeybees. Mitt Schweiz Entomol Ges 47:307–313Google Scholar
  53. Sakagami SF (1953) Untersuchungen über die Arbeitsteilung in einem Zwergvolk der Honigbienen. Beiträge zur Biologie des Bienenvolkes, Apis mellifera L. I. Jpn J Zool 11:117–185Google Scholar
  54. SAS Institute Inc. (1985) SAS user's guide: Statistics. Carry, North CarolinaGoogle Scholar
  55. Sasagawa H, Sasaki M, Okada I (1989) Hormonal control of the division of labor in adult honeybees (Apis mellifera L.) I. Effect of methoprene on corpora allata and hypopharyngeal gland, and its α-glucosidase activity. Appl Entomol Zool 24:66–77Google Scholar
  56. Seeley TD (1979) Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol 5:391–415Google Scholar
  57. Seeley TD (1985) Honey bee ecology. Princeton University Press, PrincetonGoogle Scholar
  58. Seeley TD (1989) Social foraging in honey bees: how nectar foragers assess their colony's nutrit ional status. Behav Ecol Sociobiol 24:181–99Google Scholar
  59. Simpson J (1960) The functions of the salivary glands of Apis mellifera J Insect Physiol 4:107–121Google Scholar
  60. Simpson J, Riedel IBM, Wilding N (1968) Invertase in the hypopharyngeal glands of the honeybee. J Apic Res 7:29–36Google Scholar
  61. Soudek S (1927) Hltanove Zlazy Vcely Medonosne (The pharyngeal glands of the honey bee). Bull Ecole Brno 10:1–63Google Scholar
  62. Tobe SS, Pratt GE (1974) The influence of substrate concentrations on the rate of insect juvenile hormone biosynthesis by corpora allata of the desert locust in vitro. Biochem J 144:107–33Google Scholar
  63. Van der Blom J (1992) Individual involvement in queen-attending of worker honeybees. Insectes Sociaux 39:237–249Google Scholar
  64. Visscher PK (1983) The honey bee way of death: necrophoric behaviour in Apis mellifera. Anim Behav 31:1070–1076Google Scholar
  65. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  66. Wingfield JC (1985) Short term changes in plasma levels of hormones during establishment and defense of a breeding territory in male song sparrows, Melospiza melodia. Horm Behav 19:174–187Google Scholar
  67. Wingfield JC, Wada M (1989) Male-male interactions increase both luteinizing hormone and testosterone in the song sparrow, Zonotrichia melodia: time course and possible neutral pathways. J Comp Physiol A 166:189–194Google Scholar
  68. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Z.-Y. Huang
    • 1
  • G. E. Robinson1
    • 1
  • D. W. Borst
    • 2
  1. 1.Department of EntomologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of BiologyIllinois State UniversityNormalUSA

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