Journal of Comparative Physiology B

, Volume 165, Issue 1, pp 18–28 | Cite as

Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees

  • Z. -Y. Huang
  • G. E. Robinson
Original Paper


Honey bee colonies can respond to changing environmental conditions by showing plasticity in age related division of labor, and these responses are associated with changes in juvenile hormone. The shift from nest taks to foraging has been especially well characterized; foraging is associated with high juvenile hormone titers and high rates of juvenile hormone biosynthesis, and can be induced prematurely in young bees by juvenile hormone treatment or by a shortage of foragers. However, very few studies have been conducted that study plasticity in division of labor under naturally occurring changes in the environment. To gain further insight into how the environment and juvenile hormone influence foraging behavior, we measured juvenile hormone titers and rates of biosynthesis in workers during times of the year when colony activity in temperate climates is reduced: late fall, winter, and early spring. Juvenile hormone titers and rates of biosynthesis decreased in foragers in the fall as foraging diminished and bees became less active. This demonstration of a natural drop in juvenile hormone confirms and extends previous findings when bees were experimentally induced to revert from foraging to within-hive tasks. In addition, endocrine changes in foragers in the fall are part of a larger seasonally related phenomenon in which juvenile hormone levels in younger, pre-foraging bees also decline in the fall and then increase the following spring as colony activity increases. The seasonal decline in juvenile hormone in foragers was mimicked in summer by placing a honey bee colony in a cold room for 8 days. This suggests that seasonal changes in juvenile hormone are not related to photoperiod changes, but rather to changes in temperature and/or colony social structure that in turn influence endocrine and behavioral development. We also found that active foragers in the late winter and early spring had lower juvenile hormone levels than active foragers in late spring. In light of recent findings of a possible link between juvenile hormone and neuroanatomical plasticity in the bee brain, these results suggest that bees can forage with low juvenile hormone, after previous exposure to some threshold level of juvenile hormone leads to changes in brain structure.

Key words

Corpora allata Seasonal variation Juvenile hormone Social insects Honey bee, Apis mellifera 



corpora allata


decays per minute


high performance liquid chromatography


Juvenile hormone




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the CNS. Annu Rev Neurosci 7:413–442CrossRefPubMedGoogle Scholar
  2. Banin D, Haim A, Arad Z (1994) Metabolism and thermoregulation in the levant vole Microtus guentheri—the role of photoperiodicity. J Therm Biol 19:55–62Google Scholar
  3. Breedlove SM (1992) Sexual differentiation of the brain and behavior. In: Becker JB et al (eds) Behavioral endocrinology. MIT Press, Cambridge, Mass., pp 39–70Google Scholar
  4. Burgett M, Burikam I (1985) Number of adult honey bees (Hymenoptera: Apidae) occupying a comb: a standard for estimating colony populations. J Econ Entomol 78:1154–1156Google Scholar
  5. Bühler A, Lanzrein B, Wille H (1983) Influence of temperature and carbon dioxide concentration on juvenile hormone titre and dependent parameters of adult worker honey bees (Apis mellifera L.). J Insect Physiol 29:885–893CrossRefGoogle Scholar
  6. Cherednikov AV (1967) Photoperiodism in the honey bee, Apis mellifera. Entomol Rev 46:33–37Google Scholar
  7. Davis RL (1993) Mushroom bodies and Drosophila learning. Neuron 11:1–14CrossRefPubMedGoogle Scholar
  8. Debelle JS, Heisenberg M (1994) Associate odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692–695Google Scholar
  9. De Kort CA (1990) Thirty-five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56:1–13CrossRefGoogle Scholar
  10. De Kort CA, Granger NA (1981) Regulation of the juvenile hormone titer. Annu Rev Entomol 26:1–28CrossRefGoogle Scholar
  11. De Kort CAD, Koopmanschap AB, Strambi C, Strambi A (1985) The application and evaluation of a radioimmunoassay for measuring invenile hormone titres in Colorado beetle haemolymph. Insect Biochem 15:771–775Google Scholar
  12. De Wilde J, Duintjer CA, Mook L (1959) Physiology of diapause in the adult Colorado beetle (Leptinotarsa decemlineata). I. The photoperiod as a controlling factor. J Insect Physiol 3:75–85CrossRefGoogle Scholar
  13. Eizaguirre M, Lopez C, Asin L, Albajes R (1994) Thermoperiodism, photoperiodism and sensitive stage in the diapause induction of Sesamia nonagrioides (Lepidoptera, Noctuidae). J Insect Physiol 40:113–119CrossRefGoogle Scholar
  14. Erber J, Homberg U, Gronenberg W (1987) Functional roles of the mushroom bodies in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 484–512Google Scholar
  15. Fluri P, Boganov S (1987) Effects of artificial shortening of the photoperiod on honey bee (Apis mellifera) polyethism. J Apic Res 26:83–89Google Scholar
  16. 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 28:61–68CrossRefGoogle Scholar
  17. Fluri P, Wille H, Gerig L, Lüscher M (1977) Juvenile hormone, vitellogenin and haemocyte composition in winter worker honeybees (Apis mellifera). Experientia 33:1240–1241CrossRefGoogle Scholar
  18. Frisch K von (1967) The dance language and orientation of bees. Belknap/Harvard Univ Press, Cambridge, Mass.Google Scholar
  19. 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
  20. 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
  21. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30PubMedGoogle Scholar
  22. Henley J, Greenwood J, Stout J, Atkins G (1992) Age-correlated changes and juvenile hormone III regulation of the syllable period specific responses of the L3 auditory interneurons in the cricket, Acheta domesticus. J Comp Physiol A 170:373–378CrossRefGoogle Scholar
  23. Huang Z-Y, Robinson GE (1992) Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci USA 89: 11726–11729PubMedGoogle Scholar
  24. Huang Z-Y, Robinson GE, Borst DW (1994) Physiological correlates of division of labor among similarly aged honey bees. J Comp Physiol A 174:731–739CrossRefPubMedGoogle Scholar
  25. 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 37:733–741CrossRefGoogle Scholar
  26. Hunnicutt, D, Toong YC, Borst DW (1989) A chiral specific antiserum for juvenile hormone. Am Zool 29: 48aGoogle Scholar
  27. 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
  28. 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
  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. Karp JD, Powers JB (1993) Photoperiodic and pineal influences on estrogen-stimulated behaviours in female Syrian hamsters. Physiol Behav 54:19–28CrossRefPubMedGoogle Scholar
  31. Kelly DB (1986) The genesis of male and female brains. Trends Neurosci 9:499–502Google Scholar
  32. McEwen BS, Coirini H, Westlin D, Danielsson A, Frankfurt M, Gould E, Schumacher M, Wooley C (1991) Steroid hormones as mediators of neural plasticity. J. Steroid Biochem Molec Biol 39: 223–232PubMedGoogle Scholar
  33. Merz R, Gerig L, Wille H, Leuthold R (1979) Das Problem der Kurz- und Langlebigkeit bei der Ein- und Auswinterung im Bienenvolk (Apis mellifera): Eine Verhaltensstudie. Rev Suisse Zool 86:663–671Google Scholar
  34. Milojévic BD (1940) A new interpretation of the social life of the honeybee. Bee World 21:39–41Google Scholar
  35. Moritz RFA, Southwick EE (1992) Bees as superorganisms, an evolutionary reality. Springer, Berlin HeidelbergGoogle Scholar
  36. Neukirch A (1982) Dependence of the life span of the honeybee (Apis mellifera) upon flight performance and energy consumption. J Comp Physiol A 146:35–40Google Scholar
  37. Page RE, Robinson GE (1991) The genetics of division of labour in honey bee colonies. Adv Insect Physiol 23:117–171Google Scholar
  38. Page RE, Robinson GE, Britton DS, Fondrk MK (1992) Genotypic variability for rates of behavioral development in worker honey bees (Apis mellifera). Behav Ecol 3:173–180Google Scholar
  39. Palli SR, Touhara K, Charles J-P, Bonning BC, Atkinson JK, Trowell SC, Hiruma K, Goodman WG, Kyriakides T, Prestwich GD, Hammock BD, Riddiford LM (1994) A nuclear juvenile hormone binding protein from larvae of Manduca sexta: aputative receptor for the metamorphic action of JH. Proc Natl Acad Sci USA 91:6191–6195PubMedGoogle Scholar
  40. Pellet FC (1938) History of American beekeeping. Collegiate Press, Ames, IowaGoogle Scholar
  41. Pener MP (1992) Environmental cues, endocrine factors, and reproductive diapause in male insects. Chronobiol Internat 9:102–113Google Scholar
  42. Phillips EF (1915) Beekeeping. MacMillan, New YorkGoogle Scholar
  43. Pratt GE, Tobe SS (1974) Juvenile hormones radiobiosynthesized by corpora allata of adult female locusts in vitro. Life Sci 14: 575–586CrossRefPubMedGoogle Scholar
  44. Rafaeli A, Soroker V, Hirsch J, Kamensky B, Raina AK (1993) Influence of photoperiod and age on the competence of pheromone glands and on the distribution of immunoreactive PBAN in Helicoverpa spp. Arch Insect Biochem Physiol 22: 169–180CrossRefGoogle Scholar
  45. Robinson GE (1985) Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. J Insect Physiol 31:277–282CrossRefGoogle Scholar
  46. Robinson GE (1987a) Regulation of honey bee age polyethism by juvenile hormone. Behav Ecol Sociobiol 20:329–338CrossRefGoogle Scholar
  47. 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: 613–619CrossRefGoogle Scholar
  48. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665CrossRefPubMedGoogle Scholar
  49. Robinson GE, Ratnieks F (1987) Induction of premature honey bee (Hymenoptera: Apidae) flight by juvenile hormone analogs administered orally or topically. J Econ Entomol 80:784–787Google Scholar
  50. 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: 457–459CrossRefPubMedGoogle Scholar
  51. 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
  52. 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 37:929–935CrossRefGoogle Scholar
  53. Robinson GE, Page RE, Strambi C, Strambi A (1992) Colony integration in honey bees: mechanisms of behavioural reversion. Ethology 90:336–350Google Scholar
  54. Rösch GA (1930) Untersuchungen über die Arbeitsteilung im Bienenstaat. II. Die Tätigkeiten der Arbeitsbienen unter experimentell veränderten Bedinguangen. Z Vergl Physiol 12:1–71CrossRefGoogle Scholar
  55. Sasagawa H, Sasaki M, Okada I (1986) Experimental induction of the division of labor in worker Apis mellifera L. by juvenile hormone and its analog. 30th Int Congr Apicult, Apimondia. Nagoya, pp 130–132Google Scholar
  56. Seeley TD, Visscher PK (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol 10:81–88Google Scholar
  57. Steel RGD, Torrie JH (1980) Principles and procedures of statistics, a biomedical approach. McGraw-Hill, New YorkGoogle Scholar
  58. Stout J, Atkins G, Zacharias D (1991) Regulation of cricket phonotaxis through hormonal control of the threshold of an identified auditory neuron. J Comp Physiol A 169:765–772CrossRefPubMedGoogle Scholar
  59. Stout J, Hayes V, Zacharias D, Henley J, Stumpner A, Hao J, Atkins G (1992) Juvenile hormone controls phonotactic reponsiveness of female crickets by genetic regulation of the response properties of identified auditory interneurons. In: Mauchamp B et al. (eds) Insect iuvenile hormone research: fundamental and applied approaches. Institute National Recherche Agronomique, Paris, pp 265–283Google Scholar
  60. Strambi C, Strambi A, Reggi M de, Hirn M, Delaage M (1981) Radioimmunoassay of insect juvenile hormone and of their diol derivatives. Eur J Biochem 118:401–406PubMedGoogle Scholar
  61. Tanaka S, Hakomori T, Hasegawa E (1993) Effects of daylength and hopper density on reproductive traits in a Japanese population of the migratory locust, Locusta migratoria L. J Insect Physiol 39: 571–580Google 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 144:107–133PubMedGoogle Scholar
  63. Winston ML (1987) The biology of the honey bee. Harvard Univ. Press, Cambridge, Mass.Google Scholar
  64. Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238–240CrossRefPubMedGoogle Scholar
  65. Withers GS, Fahrbach SE, Robinson GE (1995) Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J Neurobiol 26:130–144CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Z. -Y. Huang
    • 1
  • G. E. Robinson
    • 1
  1. 1.Department of EntomologyUniversity of IllinoisUrbanaUSA

Personalised recommendations