Skip to main content
SpringerLink
Log in

Histochemical and electron microscope observations on the reproductive tract of Biomphalaria glabrata (Australorbis glabratus), intermediate host of Schistosoma mansoni

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

The reproductive tract including the accessory sex glands of Biomphalaria glabrata have been studied by use of histochemical and electron microscope techniques.

The hermaphroditic part consists of glycogen containing ciliated cells. In the sparsely ciliated “secretory cells” of the vesiculae seminales, diverticula of the hermaphroditic duct, sperms are absorbed and destructed intracellularly. The observations suggest that this is a cyclic process in which lysosomes play an important role.

In the female and male part — in the tract as well as in the glands — glycogen storing ciliated cells alternate with secretory cells.

The secretory cells of the albumen gland produce galactogen and proteins. In the rest of the female part nine different secretory cell types could be distinguished on the basis of their location, the histochemical nature of the products — sulphated and non sulphated acid-mucopolysaccharides, glyco- or muco-proteins and neutral polysaccharides — and the ultrastructure of the cells. These histological findings account for the five divisions of the female tract: 1. oviduct, 2. muciparous gland, 3. oöthecal gland, 4. uterus and 5. vagina.

The ultrastructure of the cells of the bursa copulatrix suggests the production of hydrolizing enzymes for the extracellular destruction of superfluous sperms obtained by copulation.

In the spermduct and prostate gland seven different secretory cell types were found. Each cell type has its special location and ultrastructure. They produce mainly lipoproteins except for one of the cell types the product of which remained obscure.

The electron microscope observations on the penial complex revealed striking pinocytosis and loosening of the epithelium from the basement membrane in special area's. It is suggested that these phenomena play a role in erection.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdel-Malek, E. T.: Morphology, bionomics and host-parasite relations of Planorbidae (Mollusca: Pulmonata). Ph. D. Thesis, University of Michigan, 226 pp (1952).

  • —: Morphological studies on the family Planorbidae (Mollusca: Pulmonata). I. Genital organs of Helisoma trivolvis (Say) (subfamily Helisomatinae F. C. Baker, 1945). Trans. Amer. micr. Soc. 73, 103–124 (1954a).

    Google Scholar 

  • —: Morphological studies on the family Planorbidae (Mollusca: Pulmonata). II. The genital organs of Biomphalaria boissyi (subfamily Planorbinae, H. A. Pilsbry, 1934). Trans. Amer. micr. Soc. 73, 285–296 (1954b).

    Google Scholar 

  • Alaphilippe, F.: Contribution à l'étude anatomique et histologique des voies génitales de Planorbis (Planorbarius) corneus L. (Gastéropode Pulmoné). Bull. Biol. 93 (fasc. 3), 260–287 (1959).

    Google Scholar 

  • Baker, F. C.: The molluscan family Planorbidae. Urbana, Illinois: Univ. Illinois Press 1945.

    Google Scholar 

  • Baldwin, E., Bell, D. J.: Preliminary investigation of galactogen from the albumin glands of Helix pomatia. J. chem. Soc., Pt. II, 1461–1465 (1938).

  • Bayne, C. J.: Observations on the composition of the layers of the egg of Agriolimax reticulatus, the grey field slug. Comp. Biochem. Physiol. 19, 317–338 (1966).

    Google Scholar 

  • —: Studies on the composition of extracts of the reproductive glands of Agriolimax reticulatus, the grey field slug (Pulmonata, Stylommatophora). Comp. Biochem. Physiol. 23, 761–773 (1967).

    Google Scholar 

  • Boer, H. H., Lever, J.: The effect of amphenone B on the egg production of Lymnaea stagnalis. Malacologia 5 (3), 431–444 (1967).

    Google Scholar 

  • —, Wendelaar Bonga, S. E., Rooyen, N. van: Light and electron microscopical investigations on the salivary glands of Lymnaea stagnalis L. Z. Zellforsch. 76, 228–247 (1967).

    Google Scholar 

  • Bolognani Fantin, A. M., Vigo, E.: Histochemistry of the glands associated with the reproductive tract of Lymnaea stagnalis. Histochemie 15, 300–311 (1968).

    Google Scholar 

  • Bondesen, P.: A comparative morphological-biological analysis of the egg capsules of freshwater pulmonate gastropods. Hygrophila, Basomatophora, Pulmonata. Natura jutl. 3, 1–208 (1950).

    Google Scholar 

  • Bretschneider, L. H.: Insemination in Limnaea stagnalis. Proc. kon. ned. Akad. Wet. (C) 51, 358–362 (1948a).

    Google Scholar 

  • —: The mechanism of oviposition in Limnaea stagnalis. Proc. kon. ned. Akad. Wet (C) 51, 616–626 (1948b).

    Google Scholar 

  • Breucker, H.: Cytologische Untersuchungen des Zwitterganges und des Spermoviductus von Helix pomatia L. Protoplasma 58, 1–41 (1964).

    Google Scholar 

  • Correa, J. B. C., Dmytraczenko, A., Duarte, J. H.: Structure of a galactan found in the albumen gland of Biomphalaria glabrata. Carbohydrate Res. 3, 445–452 (1967).

    Google Scholar 

  • Crabb, E. D.: Anatomy and function of the reproductive system in the snail Lymnaea stagnalis appressa Say. Biol. Bull. 53, 55–66 (1927).

    Google Scholar 

  • Duncan, C. J.: The anatomy and physiology of the reproductive system of the freshwater snail Physa fontinalis (L). Proc. zool. Soc. Lond. 131, 55–84 (1958).

    Google Scholar 

  • —: The genital systems of the freshwater Basommatophora. Proc. zool. Soc. Lond. 135, 339–356 (1960).

    Google Scholar 

  • Farquhar, M. G., Palade, G. E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).

    Google Scholar 

  • Geldmacher-Mallinckrodt, M., Horstmann, H. J.: Die Polysaccharide der Weinbergschnecke. VIII. Hoppe-Seylers Z. physiol. Chem. 333, 226–231 (1963).

    Google Scholar 

  • —, May, F.: Die Polysaccharide der Weinbergschnecke. I. Hoppe-Seylers Z. physiol. Chem. 307, 179–190 (1957a).

    Google Scholar 

  • —: Die Polysaccharide der Weinbergschnecke. II. Hoppe-Seylers Z. physiol. Chem. 307, 191–201 (1957b).

    Google Scholar 

  • George, J. C., Jura, C.: A histochemical study of the capsule fluid of the egg of a land snail Succinea putris. Proc. kon. ned. Akad. Wet. 61, 598–603 (1958).

    Google Scholar 

  • Gottfried, H., Dorfman, R. I., Wall, P. E.: Steroids of invertebrates: Production of oestrogens by an accessory reproductive tissue of the slug Arion ater rufus (Linn.). Nature (Lond.) 215 (1), 409–410 (1967).

    Google Scholar 

  • Goudsmit, E. M.: The metabolism of galactogen and glycogen by pulmonate snails Bulimnaea megasoma and Helix pomatia. Ph. D. Thesis, University of Michigan (1964).

  • —, Ashwell, G.: Enzymatic synthesis of galactogen in the snail Helix pomatia. Biochem. biophys. Res. Commun. 19, 417–422 (1965).

    Google Scholar 

  • Haguenau, F.: Rôle de l'ergastoplasme dans la sécrétion. Biol. méd. (Paris) 53, 569–592 (1964).

    Google Scholar 

  • Helander, H. F.: Morphology of animal secretory gland cells. In: Sekretion und Exkretion, S. 2–21. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • Holm, L. W.: Histological and functional studies on the genital tract of Lymnaea stagnalis appressa Say. Trans. Amer. micr. Soc. 65, 45–68 (1946).

    Google Scholar 

  • Horstmann, H. J.: Untersuchungen zur Physiologie der Begattung und Befruchtung der Schlammschnecke Lymnaea stagnalis L. Z. Morph. Ökol. Tiere 44, 222–268 (1955).

    Google Scholar 

  • Hubendick, B.: The anatomy of Bulinus, with a discussion of the term prostate and its sense in the Basommatophora. Proc. Malac. Soc. Lond. 27, 186–196 (1948).

    Google Scholar 

  • Joosse, J., Boer, M. H., Cornelisse, C. J.: Gametogenesis and oviposition in Lymnaea stagnalis as influenced by γ-irradiation and hunger. Symp. zool. Soc. Lond. 22, 213–235 (1968).

    Google Scholar 

  • Jura, C., George, J. C.: Observations on the jelly mass of the eggs of three molluscs Succinea putris, Lymnaea stagnalis, and Planorbis corneus with special reference to metachromasia. Proc. kon. ned. Akad. Wet. 61, 590–594 (1958).

    Google Scholar 

  • Kugler, O. E.: A morphological and histochemical study of the reproductive system of the slug Philomycus carolinianus (Bosc.). J. Morph. 116, 117–131 (1965).

    Google Scholar 

  • Kurosumi, K.: Electron microscope analysis of the secretion mechanism. In: International review of cytology, vol. II, p. 1–117. New York and London: Academic Press 1961.

    Google Scholar 

  • Lane, N., Caro, L., Otero-Vilardebo, L. R., Godman, G. C.: On the site of sulfation in colonic goblet cells. J. Cell Biol. 21, 339–351 (1964).

    Google Scholar 

  • Lusis, O.: Postembryonic changes in the reproductive system of the slug Arion ater rufus L. Proc. zool. Soc. Lond. 137, 433–468 (1961).

    Google Scholar 

  • Mandahl-Barth, G.: Intermediate hosts of Schistosoma. African Biomphalaria and Bulinus. I. Bull. Wld Hlth Org. 16, 1103–1163 (1957a).

    Google Scholar 

  • —: Intermediate hosts of Schistosoma. African Biomphalaria and Bulinus. II. Bull. Wld Hlth Org. 17, 1–65 (1957b).

    Google Scholar 

  • May, F.: Beitrag zur Kenntnis des tierischen Sinistrins. Z. Biol. 91, 215–220 (1931).

    Google Scholar 

  • —: Beitrag zur Kenntnis des Glykogen- und Galaktogengehaltes bei Helix pomatia. Z. Biol. 92, 319–324 (1932a).

    Google Scholar 

  • —: Über den Galaktogengehalt der Eier von Helix pomatia. Z. Biol. 92, 325–330 (1932b).

    Google Scholar 

  • May, F.: Chemische und biologische Untersuchungen über Galaktogen (Chemischer Teil). Z. Biol. 95, 287–297 (1934a).

    Google Scholar 

  • —: Chemische und biologische Untersuchungen über Galaktogen (Biologischer Teil): Der Jahreszyklus in Galaktogen- und Glykogenbestand der Weinbergschnecke. Z. Biol. 95, 401–430 (1934b).

    Google Scholar 

  • —: Galaktogen- und Glykogengehalt bei hungernden Weinbergschnecken. Z. Biol. 95, 606–613 (1934c).

    Google Scholar 

  • McMahon, P., Brand, T. von, Nolan, M. O.: Observations on the polysaccharides of aquatic snails. J. cell. comp. Physiol. 50, 219–239 (1957).

    Google Scholar 

  • Morrill, J. B.: Protein content and dipeptidase activity of normal and cobalt-treated embryos of Limnaea palustris. Acta Embryol. Morph. exp. (Palermo) 7, 131–142 (1964).

    Google Scholar 

  • —, Norris, E., Smith, S. D.: Electro- and immunoelectrophoretic patterns of egg albumen of the pond snail Limnaea palustris. Acta Embryol. Morph. exp. (Palermo) 7, 155–166 (1964).

    Google Scholar 

  • Neutra, M., Leblond, C. P.: Synthesis of the carbohydrate of mucus in the Golgi complex, as shown by electron microscope radioautography of goblet cells from rats injected with glucose-H3. J. Cell Biol. 30, 119–136 (1966).

    Google Scholar 

  • —: Radioautographic comparison of the uptake of galactose-H3 and glucose-H3 in the Golgi region of various cells secreting glycoproteins or mucopolysaccharides. J. Cell Biol. 30, 137–150 (1966).

    Google Scholar 

  • Pan, C. T.: The general histology and topographic microanatomy of Australorbis glabratus. Bull. Mus. Comp. Zool. Harv. 119, 238–299 (1958).

    Google Scholar 

  • Paraense, W. L., Deslandes, N.: Observations on the morphology of Australorbis glabratus. Mem. Inst. Osw. Cruz 53, 87–103 (1955).

    Google Scholar 

  • Pearse, A. G. E.: Histochemistry. Theoretical and applied. London: I. & A. Churchill, Ltd. 1960.

    Google Scholar 

  • Pease, D. C.: Histological techniques for electron microscopy, 2nd ed. New York: Academic Press 1964.

    Google Scholar 

  • Peterson, M., Leblond, C. P.: Synthesis of complex carbohydrates in the Golgi-region as shown by autoradiography after injection of labeled glucose. J. Cell Biol. 21, 143–148 (1964).

    Google Scholar 

  • Peute, J., Kamer, J. C. van de: On the histochemical differences of aldehyd-fuchsin positive material in the fibres of the hypothalamo-hypophysial tract of Rana temporaria. Z. Zellforsch. 83, 441–448 (1967).

    Google Scholar 

  • Quattrini, D.: Struttura e ultrastruttura della prostata dei Molluschi. I. Osservazioni in Vaginulus borellianus (Colosi). Gastropoda Soleolifera. Monit. zool. ital. 74, 1–30 (1966a).

    Google Scholar 

  • —: Struttura e ultrastruttura della prostata dei Molluschi. II. Osservazioni in Laevicaulis alte (Férussac). Gastropoda Soleolifera. Monit. zool. ital. 74, 125–141 (1966b).

    Google Scholar 

  • —: Structure and ultrastructure of the molluscan prostate. III. Observations on Milax gagates (Draparnaud). Gastropoda Pulmonata Stilomatophora. Monit. zool. ital. (N.S.) 1, 109–128 (1967a).

    Google Scholar 

  • —: Structure and ultrastructure of the molluscan prostate. IV. Observations on Aplysia depilans Gmelin (Gastropoda Opistobranchia). Monit. zool. ital. (N.S.) 1, 235–259 (1967b).

    Google Scholar 

  • Rambourg, A., Hernandez, W., Leblond, L. P.: Detection of complex carbohydrates in the Golgi apparatus of rat cells. J. Cell Biol. 40, 395–414 (1969).

    Google Scholar 

  • Rangarao, K.: The composition of egg capsules of the pulmonate snail Ariophanta ligulata. Curr. Sci. 32, 213–214 (1963a).

    Google Scholar 

  • —: The polysaccharides of the reproductive system of the land snail Ariophanta ligulata in the formation of egg capsules. J. anim. Morph. Physiol. 10, 158–163 (1963b).

    Google Scholar 

  • Ravetto, C.: Alcian blue — Alcian yellow: a new method for identification of different acidic groups. J. Histochem. Cytochem. 12, 44 (1964).

    Google Scholar 

  • Rigby, J. E.: Alimentary and reproductive systems of Oxychilis cellarius. Proc. zool. Soc. Lond. 141, 311–359 (1963).

    Google Scholar 

  • —: Succinea putris: a terrestrial opistobranch mollusc. Proc. zool. Soc. Lond. 144, 445–487 (1965).

    Google Scholar 

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

    Google Scholar 

  • Runham, N. W., Laryea, A. A.: Studies on the maturation of the reproductive system of Agriolimax reticulatus (Pulmonata: Limacidae). Malacologia 7 (1), 93–108 (1968).

    Google Scholar 

  • Scharrer, B.: Recent progress in the study of neuro-endocrine mechanism in insects. Arch. Anat. micr. Morph. exp. 54, 331–342 (1965).

    Google Scholar 

  • Smith, B. J.: The secretions of the reproductive tract of the garden slug, Arion ater. Ann. N. Y. Acad. Sci. 118 (Art. 24), 997–1014 (1965).

    Google Scholar 

  • Tigyi, A., Montskó, T., Komàromy, L., Lissák, K.: Comparative ultrastructural analysis of the mechanism of secretion. Acta physiol. Acad. Sci. hung. 33 (2), 127–140 (1968).

    Google Scholar 

  • Vigo, E.: Osservazioni sui polisaccaridi presenti nella ghiandola dell' albume di Lymnaea stagnalis. Riv. Istoch. norm. pat. 13, 1–5 (1967).

    Google Scholar 

  • Wendelaar Bonga, S. E., Boer, H. H.: Ultrastructure of the reno-pericardial system in the pond snail Lymnaea stagnalis (L.). Z. Zellforsch. 94, 513–529 (1969).

    Google Scholar 

  • Zeigel, R. F., Dalton, A. J.: Speculations based on morphology of Golgi-systems in several types of protein secreting cells. J. Cell Biol. 15, 45–54 (1962).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoological Department, Free University, Amsterdam, The Netherlands

    Marijke de Jong-Brink

Authors
  1. Marijke de Jong-Brink
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The author is greatly indebted to Prof. J. Lever for his stimulating interest in the investigations, to Dr. H. H. Boer for suggesting the problem and his valuable criticism during the preparation of the manuscript, to Miss C. M. van Delft for her technical assistance, to Mr. C. van Groenigen, Mr. R. Lutgerhorst, Mr. G. W. H. van den Berg and Mr. S. E. Wendelaar Bonga for preparing the illustrations and to Mrs. D. M. Roeleveld-Bruins for typing the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Jong-Brink, M. Histochemical and electron microscope observations on the reproductive tract of Biomphalaria glabrata (Australorbis glabratus), intermediate host of Schistosoma mansoni . Z. Zellforsch. 102, 507–542 (1969). https://doi.org/10.1007/BF00335491

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00335491

Key-Words

Search

Navigation