Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Spermatogenesis and the role of Sertoli cells in the freshwater snail Biomphalaria glabrata


The various stages of spermatogenesis and the Sertoli cells of Biomphalaria glabrata were studied with histochemical and electron microscope techniques.

During spermatogenesis a manchette of microtubules is formed around the nucleus and the mid-piece of the spermatids. This manchette becomes helically coiled and probably plays an important role in the spiralisation of the nucleus and of the mitochondrial sheath. During spermatogenesis so-called chromatoid bodies (CB) occur, which consist of arginine-rich proteins. These CB disintegrate during the early spermatid stage. The results suggest that the CB are either involved in histone transition or in the formation of microtubules. The remaining cytoplasm of the spermatids is phagocytised by the Sertoli cells. Apparently this process of phagocytosis is an important part of the mechanism of spermiation.

Morphological measurements of the Sertoli cells showed that the relative volume of most organelles decrease during spermatogenesis, indicating a general decrease in cell activity. Possible functions of the Sertoli cells, such as transportation and nutrition of spermatogenic cells and hormone production, are discussed. It is concluded on the basis of the histochemical and ultrastructural observations that the Sertoli cells are involved in the nutrition of spermatogenic cells. It seems unlikely that they are hormone producing cells.

This is a preview of subscription content, log in to check access.


  1. Anderson, W.A.: Cytochemistry of sea urchin gametes. III. Acid and alkaline phosphatase activity of spermatozoa and fertilization. J. Ultrastruct. Res. 25, 1–14 (1968)

  2. Anderson, W.A., Personne, P.: The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. J. Cell Biol. 44, 29–51 (1970)

  3. Baillie, A.H., Calman, C., Ferguson, M.M., Mck. Hart, D.: Developments in steroid histochemistry. London and New York: Academic Press 1966

  4. Bara, G.: Histochemical localization of Δ5–3β-hydroxysteroid dehydrogenase in the ovaries of a teleost, Scomber scomber L. Gen. comp. Endocr. 5, 284–296 (1965)

  5. Barth, R., Jansen, G.: Über der Begriff “Kinoplasma” in der Spermiogenese von Australorbis glabratus olivaceus (Mollusca, Pulmonata, Planorbidae). Mem. Inst. Oswaldo Cruz 58, 209–228 (1960)

  6. Barth, R., Jansen, G.: Über die Formveränderungen des Golgi-Apparates während der Spermiogenese von Australorbis glabratus olivaceus (Mollusca, Pulmonata, Planorbidae). Mem. Inst. Oswaldo Cruz 59, 83–114 (1961)

  7. Bloch, D.P., Hew, H.Y.C.: Schedule of spermatogenesis in the pulmonate snail Helix aspersa, with special reference to histone transition. J. biophys. biochem. Cytol. 7, 515–531 (1960)

  8. Boer, H.H., Joosse, J.: Endocrinology. In: Pulmonates (V. Fretter and J. Peake, eds.), Vol. 1, pp. 245–302 London: Academic Press 1975

  9. Boer, H.H., Mohamed, A.M., Minnen, J. van, Jong-Brink, M. de: Effects of castration on the activity of the endocrine dorsal bodies of the fresh-water pulmonate snail Bulinus truncatus, intermediate host of Schistosoma haematobium. Neth. J. Zool. 26, 94–105 (1976)

  10. Bogitsh, B.J.: Cytochemical observations on the midpiece of the spermatozoa of the gastropod Biomphalaria glabrata. Trans. Amer. micr. Soc. 93, 211–219 (1974)

  11. Bradley, J.V.: Distribution-free statistical tests. Englewood Cliffs, N.J.: Prentice-Hall Inc. 1969

  12. Buckland-Nicks, J.A., Chia, F.S.: Spermatogenesis of a marine snail, Littorina sitkana. Cell Tiss. Res. 170, 455–475 (1976)

  13. Carr, J., Clegg, E.J., Meek, G.A.: Sertoli cells as phagocytes: an electron microscopic study. J. Anat. (Lond.) 102, 501–509 (1968)

  14. Comings, D.E., Okada, T.A.: The chromatoid body in mouse spermatogenesis: Evidence that it may be formed by the extrusion of nucleolar components. J. Ultrastruct. Res. 39, 15–23 (1972)

  15. Courtens, J.L., Loir, M.: Mise en évidence per cytochimie ultrastructurale de la migration des histones riches en lysine au cours de la spermiogenèse de bélier. J. Microscopie 24, 249–258 (1975)

  16. Coward, S.J.: Chromatoid bodies in somatic cells of the planarian: observations on their behaviour during mitosis. Anat. Rec. 180, 533–546 (1974)

  17. Eddy, E.M.: Cytochemical observations on the chromatoid body of male germ cells. Biol. Reprod. 2, 114–128 (1970)

  18. Eddy, E.M.: Fine structural observations on the form and distribution of nuage in germ cells of the rat. Anat. Rec. 178, 731–758 (1974)

  19. Fawcett, D.W., Eddy, E.M., Phillips, D.M.: Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol. Reprod. 2, 129–153 (1970)

  20. Fawcett, D.W., Phillips, D.M.: Observations on the release of spermatozoa and on changes in the head during passage through the epididymis. J. Reprod. Fertil., Suppl. 6, 405–418 (1969)

  21. Fouquet, J.P.: La spermiation et la formation des corps résiduels chez le hamster: rôles des cellules de Sertoli. J. Microscopie 19, 161–168 (1974)

  22. Gall, J.G.: Centriole replication: A study of spermatogenesis in the snail, Viviparus. J. biophys. biochem. Cytol. 10, 163–193 (1961)

  23. Gatenby, J.B.: Notes on the gametogenesis of a pulmonate mollusc: an electron microscopical study. Cellule 60, 289–300 (1960)

  24. Gomori, G.: Microscopic histochemistry. Chicago: University of Chicago Press 1952

  25. Gomot, L.: Étude du fonctionnement de l'apparail génital de l'escargot Helix aspersa par la méthode des cultures d'organes. Arch. Anat. Hist. Embr. norm. et exp. 56, 131–160 (1973)

  26. Grassé, P.P., Carasso, N., Favard, P.: Les ultrastructures cellulaires au cours de la spermiogénèse de l'escargot (Helix pomatia L.): Evolution des chromosomes, du chondriome, de l'apparail de Golgi, etc. Ann. Sci. Nat. Zool. 18, 339–380 (1956)

  27. Grillo, M.A.: Cytoplasmic inclusions resembling nucleoli in sympathetic neurons of adult rats. J. Cell Biol. 45, 100–117 (1970)

  28. Harris, P.: Structural changes following fertilization in the sea urchin eggs. Formation and dissolution of heavy bodies. Exp. Cell Res. 48, 569–581 (1967)

  29. Hurk, R. van den: The localization of steroidogenesis in the testis of oviparous and viviparous teleosts. Proc. kon. ned. Akad. Wet., Ser. C 76, 270–279 (1973)

  30. Jong-Brink, M. de: Histochemical and electron microscope observations on the reproductive tract of Biomphalaria glabrata (Australorbis glabratus), intermediate host of Schistosoma mansini. Z. Zellforsch. 102, 507–542 (1969)

  31. Jong-Brink, M. de, Wit, A. de, Kraal, G., Boer, H.H. de: A light and electron microscope study on oogenesis in the freshwater pulmonate snail Biomphalaria glabrata. Cell Tiss. Res. 171, 195–219 (1976)

  32. Joosse, J., Reitz, D.: Functional anatomical aspects of the ovotestis of Lymnaea stagnalis. Malacologia 9, 101–109 (1969)

  33. Kalt, M.R.: Ultrastructural observations on the germ line of Xenopus laevis. Z. Zellforsch. 138, 41–62 (1973)

  34. Kalt, M.R., Pinney, H.E., Graves, K.: Inhibitor induced alterations of chromatoid bodies in male germ line cells of Xenopus laevis. Cell Tiss. Res. 161, 193–210 (1975)

  35. Karavolas, H.J., Baedecker, M.L., Engel, L.L.: Human placental 17 β-estradiol dehydrogenase. V. Purification and partial characterization of the diphosphopyridine nucleotide (triphosphopyridine nucleotide)-linked enzyme. J. biol. Chem. 245, 4948–4952 (1970)

  36. Kellog, D.A., Glenner, G.G.: Histochemical localization of human term placental 17 β-oestradiol dehydrogenases: Implication for the transhydrogenase reaction. Nature (Lond.) 187, 763–764 (1960)

  37. Kessel, R.G., Beams, A.W.: Annulate lamellae and “yolk nuclei” in oocytes of the dragon fly Libellula pulchella. J. Cell Biol. 42, 185–201 (1969)

  38. Lacy, D.: The seminiferous tubule in mammals. Endeavour, 26, 101–108 (1967)

  39. Le Beux, Y.J., Langelier, P., Poirier, L.J.: Further ultrastructural data on the cytoplasmic nucleolus resembling bodies or nematosomes. Their relationship with the subsynaptic web and a cytoplasmic filamentous network. Z. Zellforsch. 118, 147–155 (1971)

  40. Lofts, B., Bern, H.A.: The functional morphology of steroidogenic tissues. In: Steroids in non-mammalian vertebrates. New York-London: Academic Press 1972

  41. Loud, A.V., Barany, W.C., Pack, B.A.: Quantitative evaluation of cytoplasmic structures in electron micrographs. Lab. Invest. 14(6), 996–1007 (1965)

  42. Merton, H.: Die Wanderungen der Geschlechtszellen in der Zwitterdrüse von Planorbis. Z. Zellforsch. 10, 527–551 (1930)

  43. Moens, P.B., Go, V.L.W.: Intercellular bridges and division patterns of rat spermatogonia. Z. Zellforsch. 127, 201–208 (1972)

  44. Monesi, V.: Spermatogenesis and the spermatozoa. In: Reproduction in mammals (C.R. Austin and R.V. Short, eds.). Book I: Germ cells and fertilization. Chapt. 3, pp. 46–84. Chambridge: Cambridge University Press 1972

  45. Nicander, L.: An electron microscopical study of cell contacts in the seminiferous tubules of some mammals. Z. Zellforsch. 83, 375–397 (1967)

  46. Notenboom, C.D., Veerdonk, F.C.G. van de, Kamer, J.C. van de: A fluorescent modification of the Sakaguchi reaction on arginine. Histochemie 9, 117–121 (1967)

  47. Novikoff, A.B., Holtzman, E.: In: Cells and organelles. Modern biology series. Holt, Rinehart and Winston, Inc. 1970

  48. Okamura, F., Nishiayama, H.: The early development of the tail and the transformation of the shape of the nucleus of the spermatid of the domestic fowl, Gallus gallus. Cell Tis. Res. 169, 345–359 (1976)

  49. Pearse, A.G.E.: Histochemistry. Theoretical and applied. London: I &A Churchill, Ltd. Vol. 1 1968, Vol. 2 1972

  50. Personne, P.: Étude cytochemique du dérivé mitochondrial du spermatozoide de la Testacelle: recherche des protéines et des lipides. J. Microscopie 4, 627 (1965)

  51. Phillips, D.M.: Comparative analysis of mammalian sperm motility. J. Cell Biol. 53, 561–573 (1972)

  52. Prentø, P., Lyon, H.: Nucleoprotein staining. An analysis of a standardized trichloroacetic acid — Fast Green FCF procedure. Histochem. J. 5, 493–501 (1973)

  53. Quattrini, D., Lanza, B.: Ricerche sulla biologia dei Veronicellidae (Gastropoda soleolifera). II Struttura della gonade, ovogenesi e spermatogenesi in Vaginulus borellianus (Colosi) e in Laevicaulis alte (Férussac). Monit. Zool. Ital. 73, 3–60 (1965)

  54. Rebhun, L.J.: Nuclear changes during spermiogenesis in a pulmonate snail. J. biophys. biochem. Cytol. 3, 509–524 (1957)

  55. Romeis, B.: Mikroskopische Technik. München-Wien: R. Oldenbourg 1968

  56. Schjeide, O.A., Nicholls, T., Graham, G.: Annulate lamellae and chromatoid bodies in the testes of a cyprinid fish (Pimephales notatus). Z. Zellforsch. 129, 1–10 (1972)

  57. Shepherd, J.G.: Activation of Saturniid moth sperm by a secretion of the male reproductive tract. J. Insect Physiol. 20, 2107–2122 (1974a)

  58. Shepherd, J.G.: Sperm activation in Saturniid moths: some aspects of the mechanism of activation. J. Insect Physiol. 20, 2321–2328 (1974b)

  59. Shepherd, J.G.: A polypeptide sperm activator from male Saturniid moths. J. Insect Physiol. 21, 9–22 (1975)

  60. Söderström, K.O., Parvinen, M.: Incorporation of [3H] uridine by the chromatoid body during rat spermatogenesis. J. Cell Biol. 70, 239–246 (1976a)

  61. Söderström, K.O., Parvinen, M.: Transport of material between the nucleus, the chromatoid body and the Golgi complex in the early spermatids of the rat. Cell Tiss. Res. 168, 335–342 (1976b)

  62. Sokal, R.R., Rohlf, F.J.: Biometry. The principles and practice of statistics in biological research. San Francisco: W.H. Freeman and company 1969

  63. Starke, F.J.: Elektronenmikroskopische Untersuchung der Zwittergonadenacini von Planorbarius corneus L. (Basommatophora). Z. Zellforsch. 119, 483–514 (1971)

  64. Stevens, B.J., Swift, H.: RNA-transport from the nucleus to cytoplasm in Chironomus salivary gland. J. Cell Biol. 31, 55–77 (1966)

  65. Sud, B.N.: Morphological and histochemical studies of the chromatoid body in the grass-snake, Natrix natrix. Quart. J. micr. Sci. 102, 51–58 (1961 a)

  66. Sud, B.N.: Morphological and histochemical studies of the chromatoid body in the grass-snake, Natrix natrix. Quart. J. micr. Sci. 102, 51–58 (196 a)

  67. Sud, B.N.: Morphological and histochemical studies of the chromatoid body and related elements in the spermatogenesis of the rat. Quart. J. micr. Sci. 102, 495–505 (1961 b)

  68. Swift, H.: The fine structure of annulate lamellae. J. biophys. biochem. Cytol. 2, 415–425 (1956)

  69. Tandler, B., Moriber, L.G.: Fine structure of the chromatoid body during spermatogenesis in the waterspider Gerris remigis (Say). Z. Zellforsch. 68, 301–307 (1965)

  70. Thiéry, J.P.: Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J. Microscopie 6, 987–1018 (1967)

  71. Thompson, T.E., Bebbington, A.: Structure and function of the reproductive organs of three species of Aplysia (Gastropoda:Opistobranchia). Malacologia 7, 347–380 (1969)

  72. Tokuyasu, K.T., Peacock, W.J., Hardy, R.W.: Dynamics of spermiogenesis in Drosophila melanogaster. II Coiling process. Z. Zellforsch. 127, 492–525 (1972)

  73. Vaughn, J.C.: The relationship of the “sphère chromatophile” to the fate of displaced histones following histone transition in rat spermatogenesis. J. Cell Biol. 31, 257–278 (1966)

  74. Vianey-Liaud, M.: Gamétogenèses et voies génitales chez le planorbe Australorbis glabratus Say (mollusque gastéropode pulmoné); description et étude expérimentale de leur contrôle. Thesis, University of Paris VI 1972

  75. Vitale-Calpe, R., Burgos, M.H.: The mechanism of spermiation in the hamster. I. Ultrastructure of spontaneous spermiation. J. Ultrastruct. Res. 31, 381–393 (1970)

  76. Walker, M., Macgregor, H.C.: Spermatogenesis and the structure of the mature sperm in Nucella lapillus (L.). J. Cell Cci. 3, 93–104 (1968)

  77. Wendelaar Bonga, S.E.: Osmotically induced changes in the activity of neurosecretory cells located in the pleural ganglia of the fresh water snail Lymnaea stagnalis (L.), studied by quantitative electron microscopy. Neth. J. Zool. 21, 127–158 (1971)

  78. Wessels, N.K.: How living cells change shape. Sci. Amer. 225, 76–82 (1971)

  79. Wilson, E.B.: A chromatoid body simulating an accessory chromosome in Pentatoma. Biol. Bull. 24, 392–411 (1913)

  80. Yasuzumi, G.: Electron microscope studies on spermiogenesis in various animal species. Int. Rev. Cytol. 37, 53–119 (1974)

  81. Yasuzumi, G., Tanaka, H.: Spermatogenesis in animals as revealed by electron microscopy. VI Researches on the spermatozoan dimorphism in a pond snail, Cipangulopaludina malleata. J. biophys. biochem. Cytol. 4, 621–632 (1958)

Download references

Author information

Correspondence to Dr. Marijke de Jong-Brink.

Additional information

The authors are greatly indebted to Prof. Dr. J. Lever and Prof. Dr. J. Joosse for reading the manuscript; to Mrs. M.J.M. Bergamin-Sassen for technical assistance; to Dr. R. van der Hurk (University of Utrecht) for performing the reactions for steroidogenic enzymes; to Mr. R.P. Heyman, Mr. A.W.J. van Leyen and Mr. N.J.C. van Ormondt for cooperation in performing the morphometrical measurements; to Dr. J.C. de Jager and Mrs. N. Middelburg-Frielink for statistical advice; to Mr. G.W.H. van den Berg for drawing the figures; to Miss B.E.C. Plesch for correcting the English text, and to Mrs. P.F.M. Ohr-Bulder for typing the manuscript

Rights and permissions

Reprints and Permissions

About this article

Cite this article

de Jong-Brink, M., Boer, H.H., Hommes, T.G. et al. Spermatogenesis and the role of Sertoli cells in the freshwater snail Biomphalaria glabrata . Cell Tissue Res. 181, 37–58 (1977).

Download citation

Key words

  • Spermatogenesis
  • Biomphalaria glabrata
  • Chromatoid body
  • Spermiation
  • Sertoli cells