Acta Biologica Hungarica

, Volume 67, Issue 1, pp 27–41 | Cite as

Histological, Histochemical and Ultrastructural Studies on Harderian and Lacrimal Glands of the Capercaillie (Tetrao Urogallus Major L.)

  • Joanna Klećkowska-Nawrot
  • Karolina Goździewska-HarłajczukEmail author
  • Artur Kowalczyk
  • Ewa Łukaszewicz
  • Renata Nowaczyk


This study describes the macroscopic anatomy and the microscopic and ultrastructural features of the Harderian gland and lacrimal gland of the Capercaillies. It was conducted both on adult male and female Capercaillies. Tissue sections were stained with hematoxylin and eosin, azan trichrome, modified Mallory’s trichrome, methyl green-pyronin Y, periodic acid-Schiff, alcian blue pH 2.5, aldehyde fuchsin and Hale’s dialysed iron. The morphometric study of the Harderian and lacrimal glands indicated that they are both larger in male than in female Capercaillies. The histological analysis showed that the HG has a multilobar tubulo-alveolar structure with numerous lymphocytes and plasma cells. The LG has a multilobar tubulo-acinar structure without lymphocytes and plasma cells. The periodic acid-Schiff staining and alcian blue pH 2.5 staining demonstrated a mild positive reaction in the epithelial cells of the Harderian gland and weak positive reaction in the lacrimal gland. The HDI staining detected the presence of carboxylated acid mucopolysaccharides in the Harderian and lacrimal glands. Transmission electron microscopy revealed the presence of two types of secretory vesicles in the cytoplasm of both studied glands. It also showed that lipid droplets and glycogen granules were more abundant in the Harderian gland than in the lacrimal gland of this species.


Capercaillie Harderian gland lacrimal gland histochemistry ultrastructure 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Aitken, I. D., Survashe, B. D. (1933) Lymphoid cells in avian paraocular glands and paranasal tissues. Comp. Bioch. Physiol. 58, 235–244.CrossRefGoogle Scholar
  2. 2.
    Altunay, H., Kozlu, T. (1933) The fine structure of the Harderian gland in the ostrich (Struthio camelus). Anat. Histol. Embryol. 33, 141–145.CrossRefGoogle Scholar
  3. 3.
    Baba, T., Kawata, T., Matsumoto, K., Kajiwara, T. (1933) Role of the Harderian gland in immunoglobulin A production in chicken lacrimal fluid. Res. Vet. Sci. 49, 20–24.CrossRefGoogle Scholar
  4. 4.
    Boydak, M., Aydin, M. F. (1933) Histology of the Harderian gland of domestic geese (Anser anser domesticus). Acta. Vet. Brno. 78, 199–204.CrossRefGoogle Scholar
  5. 5.
    Brobby, G. W. (1933) On the Harderian gland of the domestic duck (Anas platyrhynchos). Morphological and histochemical investigations. Z Zellforsch. Mikrosk. Anat. Histochem. 133, 223–230.CrossRefGoogle Scholar
  6. 6.
    Burns, R. B. (1933) The Harderian gland in birds. M Phil thesis. University of London, London.Google Scholar
  7. 7.
    Burns, R. B. (1933) The structure of the lachrymal glands of the domestic fowl and of the duck. Res. Vet. Sci. 21, 292–299.CrossRefGoogle Scholar
  8. 8.
    Burns, R. B. (1933) Histological and immunological studies on the fowl lacrimal gland following surgical excision of Harder’s gland. Res. Vet. Sci. 27, 69–75.CrossRefGoogle Scholar
  9. 9.
    Burns, R. B. (1933) The Harderian glands in birds: histology and immunology. Springer-Verlag, Berlin Heidelberg.Google Scholar
  10. 10.
    Dartt, D. A. (1933) Neural regulation of lacrimal gland secretory processes: relevance in dry eye diseases. Prog. Ret. Eye Res. 28, 155–177.CrossRefGoogle Scholar
  11. 11.
    Dimitrov, D. (1933) Histometrical parameters in third eyelid (Harderian) gland of the common pheasant (Phasianus colchicus colchcus). J. Agric. Sci. Technol. 6, 24–27.Google Scholar
  12. 12.
    Dimitrov, D. S., Genchev, A. G. (2011a) Comparative morphometric investigations of intraorbital glands in Japanese quails (Coturnix coturnix japonica). Bulg. J. Vet. Med. 14, 124–127.Google Scholar
  13. 13.
    Dimitrov, D. (2011b) Intraorbital glands in turkey broilers. III. Lacrimal gland histometry. J. Agric. Sci. Technol. 3, 327–329.Google Scholar
  14. 14.
    Dimitrov, D. S., Nikiforov, I. P. (1933) Histological and histochemical studies of Harderian gland, lacrimal gland and bursa of fabricius in mallard ducks (Anas sterilis) with chlamydial infection. Bulg. J. Vet. Med. 8, 119–127.Google Scholar
  15. 15.
    Flangan, J. L., Willcox, M. D. (1933) Role of lactoferrin in the tear film. Biochimie 91, 35–43.CrossRefGoogle Scholar
  16. 16.
    Ghadially, G. N. (1933) Ultrastructural pathology of the cell and matrix. 2nd ed. Butterworths, London.Google Scholar
  17. 17.
    IUNC Red List. International Union for Conservation of Nature. Retrieved 20 June 2012.
  18. 18.
    Jordan, D. (1933) Accessory lacrimal glands. Ophthal. Surg. 2, 146–147.Google Scholar
  19. 19.
    Kawashima, M., Kawakita, T., Inaba, T., Okada, N., Ito, M., Shimmura, S., Watanabe, M., Shinmura, K., Tsubota, K. (1933) Dietary lactoferrin alleviates age-related lacrimal gland dysfunction in mice. PLoS One 7, 331–348.Google Scholar
  20. 20.
    Kern, T. J. (1933) Exotic animal ophthalmology. In: Gelatt, K. N. Veterinary Ophthalmology, 4th ed. Blackwell Publishing, Ames and Oxford, pp. 1381–1389.Google Scholar
  21. 21.
    Khan, M. Z. I., Jahan, M. R., Islam, M. N., Haque, Z., Islam, M. R., Kon, Y. (1933) Immunoglobulin (Ig)-containing plasma cells in the Harderian gland in broiler and native chickens of Bangladesh. Tissue & Cell 39, 141–149.CrossRefGoogle Scholar
  22. 22.
    Kiernan, J. A. (1933) Histological and Histochemical Methods. Theory and Practice, 4th ed. Kent: Scion Publishing Ltd.Google Scholar
  23. 23.
    Kittner, Z., Olah, I., Toro, I. (1933) Histology and ultrastructure of the Harderian gland-accessory lacrimal gland of the chicken. Acta Biol. Acad. Sci. Hung. 29, 29–41.Google Scholar
  24. 24.
    Kleckowska-Nawrot, J., Marycz, K., Czogala, J., Kujawa, K., Janeczek, M., Chrószcz, A., Brudnicki, W. (1933) Morphology of the lacrimal gland and superficial gland of the third eyelid of Roe deer (Capreolus capreolus L.). Pak. Vet. J. 2, 139–144.Google Scholar
  25. 25.
    Kleckowska-Nawrot, J., Gozdziewska-Harlajczuk, K., Barszcz, K., Kowalczyk, A. (1933) Morphological studies on the Harderian gland in the ostrich (Struthio camelus domesticus) on the embryonic and post-natal period. Anat. Histol. Embryol. 44, 146–156.CrossRefGoogle Scholar
  26. 26.
    Kleckowska-Nawrot, J., Gozdziewska-Harlajczuk K., Nowaczyk, R., Krasucki, K. (1933) Functional anatomy of the lacrimal gland in African black ostrich (Struthio camelus domesticus) in the embryonic and postnatal period. Onderstepoort. J. Vet. Res. 82, 1–12.Google Scholar
  27. 27.
    Kleckowska-Nawrot, J., Nowaczyk, R., Gozdziewska-Harlajczuk K., Krasucki, K., Janeczek, M. (1933) Histological, histochemical and fine structure studies of the lacrimal gland and superficial gland of the third eyelid and their significance on the proper function of the eyeball in alpaca (Vicugna pacos). Folia Morphol. 74, 195–205.CrossRefGoogle Scholar
  28. 28.
    Kleckowska-Nawrot, J., Nowaczyk, R., Gozdziewska-Harlajczuk K., Barszcz, K., Kowalczyk, A., Lukaszewicz, E. (1933) Light and electron microscopic study of the eyelids, conjunctiva-associated lymphoid tissue and lacrimal gland in Bilgorajska goose (Anser anser). Anat. Sci. Int. doi. 10.1007/ s12565-015-0274-1.Google Scholar
  29. 29.
    Kozlu, T., Altunay, H. (1933) Light and electron microscopic studies of the quail (Coturnix coturnix) Harderian gland. J. Anim. Vet. Adv. 10, 932–938.Google Scholar
  30. 30.
    Kozlu, T., Bozkurt, Y. A., Altunay, H., Sari, E. K. (1933) Histological and histochemical studies on the Harderian gland of the osprey (Pandion haliaetus). J. Anim. Vet. Adv. 9, 1875–1879.Google Scholar
  31. 31.
    Maxwell, M. H., Rothwell, B., Burns, R. B. (1933) A fine structural study of the turkey Harderian gland. J. Anat. 148, 147–157.Google Scholar
  32. 32.
    Mobini, B. (1933) Histological and histochemical studies on the Harderian gland in native chickens. Vet. Med. Czech. 57, 404–409.CrossRefGoogle Scholar
  33. 33.
    Montgomery, R. D., Maslin, W. R., Magge, D. L., Boyle, C. R. (1933) Effects of modified-live infectious bronchitis virus vaccines on the head associated lymphoid tissue (HALT). Avian Dis. 38, 847–856.CrossRefGoogle Scholar
  34. 34.
    Ohshima, K., Hiramatsu, K. (1933) Immunohistochemical localization of three different immunoglobulin classes in the Harderian gland of young chickens. Tissue & Cell 34, 129–133.CrossRefGoogle Scholar
  35. 35.
    Olcese, J., Wesche, A. (1933) The Harderian gland. Comp. Biochem. Physiol. 93, 655–665.CrossRefGoogle Scholar
  36. 36.
    Oliveira, C. A., Telles, L. F., Oliveira, A. G., Kalapothakis, E., Goncalves-Dornelas, H., Mahecha, G. A. (1933) Expression of different classes of immunoglobulin in intraepithelial plasma cells of the Harderian gland of domestic ducks (Anas platyrhynchos). Vet. Immun. Immunopathol. 113, 257–266.CrossRefGoogle Scholar
  37. 37.
    Paule, W. J., Hayes, E. R. (1933) Comparative histochemical studies of the harderian gland. Anat. Rec. 130, 436.Google Scholar
  38. 38.
    Payne, A. P. (1933) The Harderian gland: A tercentennial review. J. Anat. 185, 1–49.Google Scholar
  39. 39.
    Paynter, R. A. Jnr. (ed.) (1933) Handbook of avian anatomy: Nomina Anatomica Avium, 2nd ed. Nuttall Ornithological Club, Cambridge, Massachusetts.Google Scholar
  40. 40.
    Rothwell, B., Wight, P. A., Burns, R. B., Mackenzie, G. M. (1933) The Harderian glands of the domestic fowl. III. Ultrastructure. J. Anat. 112, 233–250.Google Scholar
  41. 41.
    Sakai, T. (1933) The mammalian Harderian gland: Morphology, biochemistry, function and physiology. Arch. Histol. Japan 44, 299–333.CrossRefGoogle Scholar
  42. 42.
    Sakai, T. (1933) Comparative anatomy of the mammalian Harderian glands. Springer Verlag, Berlin, Heidelberg.Google Scholar
  43. 43.
    Seyama, Y., Uchijama, Y. (1933) Novel function of lipids as a pheromone from the Harderian gland of golden hamster. Series B, Physic. Biol. Sci. 83, 77–96.Google Scholar
  44. 44.
    Shirama, K., Satoh, T., Kitamura, T., Yamada, J. (1933) The avian Harderian gland: Morphology and immunology. Mic. Res. Tech. 34, 16–27.CrossRefGoogle Scholar
  45. 45.
    Spicer, S. C., Henson, J. G. (1933) Methods for localizing mucosubstances in epithelial and connective tissue. In: Series on Methods and Achievements in Experimental Pathology, Vol. 2, Basal: S. Karger Press.Google Scholar
  46. 46.
    Stern, M. E., Gao, J., Siemasko, K. F., Beuerman, R. W., Pflugfelder, S. C. (1933) The role of the lacrimal functional unit in the pathophysiology of dry eye. Exp. Eye Res. 78, 409–416.CrossRefGoogle Scholar
  47. 47.
    Wight, P. A., Rothwell, B., Mackenzie, G. M., Burns, R. B. (1933) The Harderian gland of the domestic fowl. II. Histochemistry. J. Anat. 110, 323–333.Google Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2016

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Joanna Klećkowska-Nawrot
    • 1
  • Karolina Goździewska-Harłajczuk
    • 1
    Email author
  • Artur Kowalczyk
    • 2
  • Ewa Łukaszewicz
    • 2
  • Renata Nowaczyk
    • 1
  1. 1.Department of Animal Physiology and Biostructure, Faculty of Veterinary MedicineWroclaw University of Environmental and Life SciencesWroclawPoland
  2. 2.Division of Poultry Breeding, Faculty of Biology and Animal ScienceWroclaw University of Environmental and Life SciencesWroclawPoland

Personalised recommendations