Hypopharyngeal glands

honey bee hypopharyngeal glands

Dissected hypopharyngeal glands of honey bee worker.


Hypopharyngeal glands consist of a pair of long glands coiled in the sides of the head (see also side view of the glands). Each gland consists about 550 oval acini attached to an axial collecting duct [1]. Diameter of the collecting duct is approximately 60 micrometers. It is covered inside with cuticle. The ducts open on the suboral plate of hypopharynx. For detailed description of ultrastructure see [2][3][4][5][6][7][8][9][10][11][12].
Activity of the glands depends on age of workers [13][14][15], their food and presence of larvae [16][17][18]. The glands are most active in young bees, however, they can be also developed in old workers if young workers are absent, for example in hopelessly queenless colony [19]. The hypopharyngeal glands are active only in workers which have direct contact with brood [20]. There are some studies related to genetic control of hypopharyngeal glands development [21][22].
Secretion of the hypopharyngeal glands is rich in proteins. The secretion of young workers is important component of royal jelly [23][7][24][15]. The secretion of older workers contains sucrose hydrolysis enzymes [25][26] including alpha-glucosidase, amylase, and glucose oxidase [15][27]. There are known some genes which change their expression in hypopharyngeal glands with age [28][29][30].
Workers with developed hypopharyngeal glands consume more pollen [18].
Hypopharyngeal glands are less developed in workers starved [31][32], infected with Varroa [33], injected with juvenile hormone [34], poisoned with pesticides [35][36], soybean trypsin inhibitor [37][38][39][40], carbon dioxide [41][42] and other anaesthetics [43].

References

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  2. Beams H.W., Tahmisian T.N., Anderson E., Devine R.L. (1959) An electron microscope study on the pharyngeal glands of the honeybee. Journal of Ultrastructure Research 3:155–170.
  3. Painter T.S., Biesele J.J. (1966) The fine structure of the hypopharyngeal gland cell of the honey bee during development and secretion. Proceedings of the National Academy of Sciences of the United States of America 55:1414-1419.
  4. Cruz-Landim C., Hadek R. (1969) Ultrastructure of Apis mellifera hypopharyngeal gland., Proc 6th Int Congr IUSSI, Bern, pp. 121-130.
  5. Halberstadt K. (1970) A study of the ultrastructure and functional cycle of pharyngeal glands of the honeybee. Cytobiologie 2:341–358.
  6. Ortiz-Picon J.M., Diaz-Flores L. (1972) Etude structurale, optique, et electronique, des glandes hypopharyngiennes de Apis mellifera. Trabajos del Instituto Cajal de Investigaciones Biologicas 64:223-240.
  7. Knecht D., Kaatz H.H. (1990) Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie 21:457–468.
  8. Silva de Moraes R.L.M., Bowen I.D. (2000) Modes of cell death in the hypopharyngeal gland of the honey bee (Apis mellifera L). Cell Biology International 24:737–743.
  9. Deseyn J., Billen J. (2005) Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36:49–57.
  10. Kheyri H., Cribb B.W., Reinhard J., Claudianos C., Merritt D.J. (2012) Novel actin rings within the secretory cells of honeybee royal jelly glands. Cytoskeleton 69:1032-1039.
  11. Kheyri H., Cribb B.W., Merritt D.J. (2012) Comparing the secretory pathway in honeybee venom and hypopharyngeal glands. Arthropod Structure & Development (in press).
  12. Klose S.P., Rolke D., Baumann O. (2017) Morphogenesis of honeybee hypopharyngeal gland during pupal development. Frontiers in zoology 14:22.
  13. Rösch G.A. (1925) Untersuchungen über die Arbeitsteilung im Bienenstaat, I. Teil: Die tätigkeiten im normalen Bienenstaate und ihre Beziehungen zum Alter der Arbeitsbienen. Z. vergl. Physiol. 2:571-631.
  14. Suwannapong G., Chaiwongwattanakul S., Benbow M.E. (2010) Histochemical Comparison of the Hypopharyngeal Gland in Apis cerana Fabricius, 1793 Workers and Apis mellifera Linnaeus, 1758 Workers. Psyche: A journal of Entomology 2010:181025.
  15. Kubo T., Sasaki M., Nakamura J., Sasagawa H., Ohashi K., Takeuchi H., Natori S. (1996) Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis melliferaL.) with age and/or role. Journal of Biochemistry 119:291-295.
  16. Brouwers E.V.M. (1982) Measurement of hypopharyngeal gland activity in the honeybee. Journal of Apicultural Research 21:193-198.
  17. Brouwers E.V.M. (1983) Activation of the hypopharyngeal glands of honeybees in winter. Journal of Apicultural Research 22:137-141.
  18. Hrassnigg N., Crailsheim K. (1998) Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. Journal of Insect Physiology 44:929–939.
  19. Ohashi K., Sasaki M., Sasagawa H., Nakamura J., Natori S., Kubo T. (2000) Functional flexibility of the honey bee hypopharyngeal gland in a dequeened colony. Zoological science 17:1089–1094.
  20. Huang Z.Y., Otis G.W., Teal P.E.A. (1989) Nature of brood signal activating the protein synthesis of hypopharyngeal gland in honey bees, Apis mellifera (Apidae: Hymenoptera). Apidologie 20:455-464.
  21. Liu H., Wang Z.-L., Tian L.-Q., Qin Q.-H., Wu X.-B., Yan W.-Y., Zeng Z.-J. (2014) Transcriptome differences in the hypopharyngeal gland between Western Honeybees (Apis mellifera) and Eastern Honeybees (Apis cerana). BMC Genomics 15:744.
  22. Liu H., Wang Z.-L., Zhou L.-B., Zeng Z.J. (2015) Quantitative analysis of the genes affecting development of the hypopharyngeal gland in honey bees (Apis mellifera L.). Sociobiology 62:412–416.
  23. Halberstadt K. (1980) Elektrophoretische Untersuchungen zur Sekretionstätigkeit der Hypopharynxdrüse der Honigbiene (Apis Mellifera L.). Insectes Sociaux 27:61-77.
  24. Hanes J., Simuth J. (1992) Identification and partial characterization of the major royal jelly protein of the honey bee (Apis mellifera L.). J. Apic. Res. 31:22-26.
  25. Simpson J., Riedel I.B.M., Wilding N. (1968) Invertase in the hypopharyngeal glands of the honeybee. J. Apic. Res. 7:29-36.
  26. 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. Applied Entomology and Zoology 24:66–77.
  27. Ohashi K., Natori S., Kubo T. (1999) Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). European Journal of Biochemistry 265:127–133.
  28. Ohashi K., Sawata M., Takeuchi H., Natori S., Kubo T. (1996) Molecular cloning of cDNA and analysis of expression of the gene for alpha-glucosidase from the hypopharyngeal gland of the honeybee Apis mellifera L. Biochemical and Biophysical Research Communications 221:380–385.
  29. Ohashi K., Natori S., Kubo T. (1997) Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. European Journal of Biochemistry 249:797–802.
  30. Paerhati Y., Ishiguro S., Ueda-Matsuo R., Yang P., Yamashita T., Ito K., Maekawa H., Tani H., Suzuki K. (2015) Expression of AmGR10 of the Gustatory Receptor Family in Honey Bee Is Correlated with Nursing Behavior. PloS one 10:e0142917.
  31. Free J.B. (1961) Hypopharyngeal gland development and division of labour in honey-bee (Apis mellifera L.) colonies. Proc. Roy. Entomol. Soc. London (A) 36:5-8.
  32. 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.). Journal of Insect Physiology 35:595–602.
  33. Schneider P., Drescher W. (1987) The effect of Varroa jacobsoni on development and weight of hypopharyngeal glands and lifespan of Apis mellifera. Apidologie 18:101-110.
  34. Jaycox E.R. (1976) Behavioral changes in worker honey bees (Apis mellifera L.) after injection with synthetic juvenile hormone (Hymenoptera: Apidae). J. Kans. Entomol. Soc. 49:165-170.
  35. Heylen K., Gobin B., Arckens L., Huybrechts R., Billen J. (2011) The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42:103–116.
  36. Hatjina F., Papaefthimiou C., Charistos L., Dogaroglu T., Bouga M., Emmanouil C., Arnold G. (2013) Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo. Apidologie (in press).
  37. Sagili R.R., Pankiw T., Zhu-Salzman K. (2005) Effects of soybean trypsin inhibitor on hypopharyngeal gland protein content, total midgut protease activity and survival of the honey bee (Apis mellifera L.). Journal of insect Physiology 51:953–957.
  38. Babendreier D., Kalberer N.M., Romeis J., Fluri P., Mulligan E., Bigler F. (2005) Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie 36:585-594.
  39. Sagili R.R., Pankiw T. (2007) Effects of protein-constrained brood food on honey bee (Apis mellifera L.) pollen foraging and colony growth. Behavioral Ecology and Sociobiology 61:1471–1478.
  40. Han P., Niu C.Y., Biondi A., Desneux N. (2012) Does transgenic Cry1Ac+ CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L.(Hymenoptera, Apidae)? Ecotoxicology 21:2214-2221.
  41. Fyg W. (1950) Beobachtungen über die Wirkungen der Kohlensäure-Narkose auf Arbeitsbienen. Schweizerische Bienen-Zeitung 73:174–184.
  42. Skowronek W., Jaycox E.R. (1974) Effect of carbon dioxide on the honeybee workers. Pszczelnicze Zeszyty Naukowe 18:107-119.
  43. Simpson J. (1954) Effects of some anaesthetics on honeybees: nitrous oxide, carbon dioxide, ammonium nitrate smoker fumes. Bee World 35:149–155.