Summary
The epidermis and the associated subepidermal gland cells of the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi were studied by means of histochemical and electron microscope techniques.
The single cell layered epidermis is composed of general epidermal cells, cilia cells and a few scattered goblet cells. The foot sole and the epidermal regions of the pneumostome and the ventral surface of the lips near the mouth consist nearly entirely of cilia cells; elsewhere the cilia cells are found scattered among the general epidermal cells.
The apical layer of the general epidermal cells bear microvilli. Numerous mitochondria, vesicles and lysosomes are located in the apical region of the cells. Several Golgi bodies and a poorly developed granular endoplasmic reticulum occur in the supranuclear region; the nucleus lies in the basal part of the cell. The general epidermal cells in the mouth region contain numerous microfilaments compared to the general epidermal cells in the rest of the epidermis. The cilia of the cilia cells in the densely ciliated regions possess well developed roots and basal bodies interconnected by means of the basal feet. With regard to the other cell organelles, cilia cells are quite similar to the general epidermal cells. For comparison a brief study of the ultrastructure of the epidermis of the terrestrial snail Helix aspersa was carried out.
The skin of the snail is covered by a mucous layer produced by various gland cells. In L. stagnalis, in addition to the epidermal goblet cells, thirteen subepidermal gland cell types could be distinguished. The histochemistry of the gland cell types is reflected in the ultrastructure. Three of the gland cell types have an ubiquitous distribution, four types are peculiar to the foot, two types to the lips and five types to the mantle. In B. pfeifferi one epidermal gland cell type and only seven subepidermal gland cell types could be distinguished. Most of these gland cells are limited in their distribution to the foot, lips and mantle edge.
The observations may provide a basis for further study in the functions of the snail epidermis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aardt, W. J. van: Quantitative aspects of the water balance in Lymnaea stagnalis (L.). Neth. J. Zool. 18, 253–312 (1968).
Arcadi, J. A.: Some mucus-producing cells of the garden slug (Lehmania poirieri). Ann. N.Y. Acad. Sci. 106, 451–457 (1963).
Arcadi, J. A.: Histochemical observations on the regeneration of some mucus producing cells in the integument of the garden slug Lehmania poirieri Mabille. Ann. N.Y. Acad. Sci. 118, 987–996 (1965).
Baecker, R.: Die Mikromorphologie von Helix pomatia und einigen anderen Stylommatophoren. Ergebn. Anat. Entwickl.-Gesch. 29, 449–585 (1932).
Barber, V. C., Wright, D. E.: The fine structure of the eye and optic tentacles of the mollusc Cardium edule. J. Ultrastruct. Res. 26, 515–528 (1969).
Barr, R. A.: Some notes on the mucous and skin glands of Arion ater. Quart. J. micr. Sci. 71, 503–526 (1928).
Bolognani Fantin, A. M.: La mucinogenesi nei Molluschi. I. Introduzione. Riv. Istoch. norm. pat. 13, 311–322 (1967).
Bolognani Fantin, A. M., Vigo, E.: Dati histochimici sui tipi cellulari dell' epitelio tegumentale del piede di gasteropodi acquatici. Rend. Ist. Lomb. Sc. e Lett. 101, 99–116 (1967a).
Bolognani Fantin, A. M., Vigo, E.: La mucinogenesi nei Molluschi. IV. Caratteristiche istochimiche dei tipi cellulari presenti nel piede e nel mantello di alcune specie di Gasteropodi. Riv. Istoch. norm. pat. 13, 1–28 (1967b).
Borght,, O. van der, Puymbroeck, S. van: Initial uptake, distribution and loss of soluble 106Ru in marine and freshwater organisms in laboratory conditions. Hlth Phys. 19, 801–811 (1970).
Bullivant, S., Loewenstein, W. R.: Structure of coupled and uncoupled cell junctions. J. Cell Biol. 37, 621–632 (1968).
Burkhardt, F.: Das Körperepithel von Helix pomatia L. Inaug.-Diss. Marburg (1916).
Campion, M.: The structure and function of the cutaneous glands in Helix aspersa. Quart. J. micr. Sci. 102, 195–216 (1961).
Chetail, M., Binot, D.: Particularités histochimiques de la glande et de la sole pédieuses d'Arion rufus (Stylommatophora: Arionidae). Malacologia 5, 269–284 (1967).
Danilova, L. V., Rokhlenko, K. D., Bodryagina, A. V.: Electron microscopic study on the structure of septate and comb desmosomes. Z. Zellforsch. 100, 101–117 (1969).
Diamond, J. M., Bossert, W. H.: Standing-gradient osmotic flow. A mechanism for coupling of water and solute transport in epithelia. J. gen. Physiol. 50, 2061–2083 (1967).
Elves, M. W.: The histology of the foot of Discus rotundatus, and the locomotion of gastropod Mollusca. Proc. Malac. Soc. (Lond.) 34, 346–355 (1961).
Farquhar, M. G., Palade, G. E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).
Fawcett, D. W.: Cilia and flagella. In: The cell, vol. II, p. 217–297. New York: Academic Press 1961.
Fawcett, D. W., Porter, K. R.: A study of the fine structure of ciliated epithelia. J. Morph. 93, 221–282 (1954).
Flower, N. E.: Frozen-etched septate junctions. Brief report. Protoplasma (Wien) 70, 479–483 (1970).
Gibbons, I. R.: The relationship between the fine structure and the direction of beat in gill cilia of a lamellibranch mollusc. J. biophys. biochem. Cytol. 11, 179–204 (1961).
Gibbons, I. R.: The structure and composition of cilia. In: Formation and fate of cell organelles. Symp. Int. Soc. Cell Biol. 6, 99–114 (1967).
Gilula, N. B., Branton, D., Satir, P.: The septate junction: a structural basis for intercellular coupling. Proc. nat. Acad. Sci. (Wash.) 67, 213–220 (1970).
Greenaway, P.: Sodium regulation in the freshwater mollusc Limnaea stagnalis (L.) (Gastropoda: Pulmonata). J. exp. Biol. 53, 147–163 (1970).
Greenaway, P.: Calcium regulation in the freshwater mollusc, Limnaea stagnalis (L.) (Gastropoda: Pulmonata). J. exp. Biol. 54, 199–214 (1971).
Herfs, A.: Die Haut der Schnecken in ihrer Abhängigkeit von der Lebensweise. Naturw. Wschr. 20, 601–608 (1921).
Herfs, A.: Studien an den Hautdrüsen der Land- und Süßwassergastropoden. Arch. mikr. Anat. 96, 1–38 (1922).
Hess, O.: Die Haut der Mollusken. Studium gen. 17, 161–176 (1964).
Hillman, R. E.: Formation of the periostracum in Mercenaria mercenaria. Science 134, 1754–1755 (1961).
Hubendick, B.: On the molluscan adhesive epithelium. Ark. Zool. 11, 31–36 (1958).
Hyman, L. H.: The invertebrates, vol. VI: Mollusca I. New York: McGraw-Hill 1967.
Jager, J. C.: A quantitative study of a chemoresponse to sugars in Lymnaea stagnalis (L.). Neth. J. Zool. 21, 1–59 (1971).
Jones, I. D.: Aspects of respiration in Planorbis corneus and Lymnaea stagnalis L. (Gastropoda: Pulmonata). Comp. Biochem. Physiol. 4, 1–29 (1961).
Keynes, R. D.: From frog skin to sheep rumen: a survey of transport of salts and water across multicellular structures. Quart. Rev. Biophys. 2, 177–281 (1969).
Kress, A.: Untersuchungen zur Histologie, Autotomie und Regeneration dreier Doto-Arten Doto coronata, D. pinnatifada, D. fragilis (Gastropoda, Opistobranchiata). Rev. suisse Zool. 75, 235–303 (1968).
Lane, N. J.: Microvilli on the external surfaces of gastropod tentacles and body-walls. Quart. J. micr. Sci. 104, 495–504 (1963).
Lev, R., Spicer, S. S.: Specific staining of sulphate groups with alcian blue at low pH. J. Histochem. Cytochem. 12, 309 (1964).
Lever, J., Bekius, R.: On the presence of an external hemal pore in Lymnaea stagnalis L. Experientia (Basel) 21, 395 (1965).
Lever, J., Jager, J. C., Westerveld, A.: A new anaesthetization technique for freshwater snails, tested on Lymnaea stagnalis. Malacologia 1, 331–337 (1964).
Leydig, F.: Die Hautdecke und Schale der Gastropoden nebst einer Übersicht der einheimischen Limacinen. Arch. Naturg. 42, 209–292 (1876).
Lin, H. S.: The fine structure and transformation of centrioles in the rat pinealocyte. Cytobios 2, 129–151 (1970).
Locke, M.: The structure of septate desmosomes. J. Cell Biol. 25, 166–169 (1965).
Loewenstein, W. R.: Permeability of membrane junctions. Ann. N.Y. Acad. Sci. 137, 441–472 (1966).
Loewenstein, W. R., Kanno, Y.: Studies on an epithelia (gland) cell junction. I. Modifications of surface membrane permeability. J. Cell Biol. 22, 565–586 (1964).
Machin, J.: The evaporation of water from Helix aspersa L. The nature of the evaporating surface. J. exp. Biol. 41, 759–769 (1964).
Martoja, M., Bassot, J. M.: Étude histologique du complexe glandulaire pédieux de Dyakia striata Godwin et Austin Gastéropode Pulmoné. Données sur l'organe lumineux. Vie et Milieu, sér. A 21, 395–452 (1970).
Mukherjee, T. M., Staehelin, L. A.: The fine-structural organization of the brush border of intestinal epithelial cells. J. Cell Sci. 8, 573–599 (1971).
Pan, C. T.: The general histology and topographic microanatomy of Australorbis glabratus. Bull. Mus. Comp. Zool. Harv. 119, 238–299 (1958).
Pearse, A. G. E.: Histochemistry. Theoretical and applied. London: I. & A. Churchill, Ltd. 1960.
Pease, D. C.: Histological techniques for electron microscopy, 2nd ed. New York: Academic Press 1964.
Rasmussen, H.: Cell communication, calcium ion, and cyclic adenosine monophosphate. Science 170, 404–412 (1970).
Ravetto, C.: Alcian blue-Alcian yellow: a new method for identification of different acidic groups. J. Histochem. Cytochem. 12, 44–45 (1964).
Renault, L.: Existence d'une glande intra-palléale et d'une branchie anale chez Cassidula labrella Deshayes (Mollusque pulmoné). C. R. Acad. Sci. (Paris) 262, 2243–2245 (1966).
Renzoni, A.: Osservazioni istologische, istochimiche ed ultrastrutturali sui tentacoli di Vaginulus borrelianus (Colosi), Gastropoda Soleolifera. Z. Zellforsch. 87, 350–376 (1968).
Rogers, D. C.: Surface specializations of the epithelial cells at the tip of the optic tentacle, dorsal surface of the head and ventral surface of the foot in Helix aspersa. Z. Zellforsch. 114, 106–116 (1971).
Romeis, B.: mikroskopische Technik, 18. Aufl. München-Wien: R. Oldenbourg 1968.
Rosenberg, M. D.: Intracellular transport fluxes—can they be accurately determined? In: Intracellular Transport. Symp. Int. Soc. Cell Biol. 5, 45–70 (1966).
Roth, H.: Zur Kenntnis des Epithels und der Entwicklung der einzelligen Hautdrüsen von Helix pomatia. Z. wiss. Zool. 135, 357–427 (1929).
Sade, J., Eliezer, N., Silberberg, A., Nevo, A. C.: The role of mucus in transport by cilia. Amer. Rev. resp. Dis. 102, 48–52 (1970).
Satir, P., Gilula, N. B.: The cell junction in a lamellibranch gill ciliated epithelium. Localization of pyroantimonate precipitate. J. Cell Biol. 47, 468–487 (1970).
Schmekel, L., Wechsler, W.: Elektronenmikroskopische Untersuchungen über Struktur und Entwicklung der Epidermis von Trinchesia granosa (Gastr. Opisthobranchia). Z. Zellforsch. 77, 95–114 (1967).
Scott, J. E.: Ion binding in solutions containing acid mucopolysaccharides. In: Quintarelli, G., The chemical physiology of mucopolysaccharides. Birmingham: Univ. Alabama Med. Center 1968.
Siebert, W.: Das Körperepithel von Anodonta cellensis. Z. wiss. Zool. 106, 449–526 (1913).
Sorvari, T. E., Sorvari, R. M.: The specificity of alcian blue pH 1.0 alcian yellow pH 2.5 staining in the histochemical differentiation of acidic groups in mucosubstances. J. Histochem. Cytochem. 17, 291–293 (1969).
Starmühlner, F.: Die Gastropoden der Madagassischen Binnengewässer. Malacologia 8, 1–434 (1969).
Steen, W. J. van der, Hoven, N. P. van den, Jager, J. C.: A method for breeding and studying freshwater snails under continuous water change with some remarks on growth and reproduction in Lymnaea stagnalis (L.) Neth. J. Zool. 19, 131–139 (1969).
Threadgold, L. T.: The ultrastructure of the animal cell. Oxford: Pergamon Press 1967.
Tilney, L. G., Mooseker, M.: Actin in the brush-border of epithelial cells of the chicken intestine. Proc. nat. Acad. Sci. (Wash.) 68, 2611–2615 (1971).
Timmermans, L. P. M.: Studies on shell formation in molluscs. Neth. J. Zool. 19, 417–523 (1969).
Vlieger, T. A. de: An experimental study of the tactile system of Lymnaea stagnalis (L.). Neth. J. Zool. 18, 105–154 (1968).
Welsch, U.: Beobachtungen über die Feinstruktur der Haut und des äußeren Atrialepithels von Branchiostoma lanceolatum Pall. Z. Zellforsch. 88, 565–575 (1968).
Welsch, U., Storch, V.: Zum Aufbau und zur Innervation des Wimperepithels der Bivalvia-Palpen. Z. Zellforsch. 97, 383–391 (1969).
Wendelaar Bonga, S. E.: Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stagnalis (L.). Z. Zellforsch. 108, 190–224 (1970).
Wessels, N. K., Spooner, B. S., Ash, J. F., Bradley, M. O., Luduena, M. A., Taylor, E. L., Wrenn, J. T., Yamada, K. M.: Microfilaments in cellular and developmental processes. Science 171, 135–143 (1971).
Williams, T.: The staining of nervous elements by the Bodian method. I. The influence of factors preceding impregnation. Quart. J. micr. Sci. 103, 155–162 (1962).
Wondrak, G.: Die exoepithelialen Schleimdrüsenzellen von Arion empiricorum (Fér). Z. Zellforsch. 76, 287–294 (1967).
Wondrak, G.: Elektronenoptische Untersuchungen der Körperdecke von Arion rufus L. (Pulmonata.) Protoplasma (Wien) 66, 151–171 (1968).
Wondrak, G.: Elektronenoptische Untersuchungen der Drüsen- und Pigmentzellen aus der Körperdecke von Arion rufus (L.) (Pulmonata). Z. mikr.-anat. Forsch. 80, 17–40 (1969).
Wood, R. L.: Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J. biophys. biochem. Cytol. 6, 343–351 (1959).
Zaaijer, J. J. P., Wolvekamp, H. P.: Some experiments on the haemoglobin-oxygen equilibrium in the blood of the ramshorn (Planorbis corneus L.). Acta physiol. pharmacol. neerl. 7, 56–77 (1958).
Zylstra, U.: Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Neth. J. Zool. 22, 283–298 (1972).
Author information
Authors and Affiliations
Additional information
The author is greatly indebted to Prof. Dr. J. Lever for suggesting the problem and for his advice during the investigation, to Dr. H. H. Boer for his guidance and valuable criticism in the preparation of the manuscript, to Mrs. N. van Zwieten-Laman for technical assistance, to Mr. G. Elisée-Desir, Mr. J. H. Huysing, Mr. R. Lutgerhorst, and Mr. C. van Groenigen for preparing the micrographs, to Mr. G. W. H. van den Berg for preparing the illustrations and to Mrs. J. H. Buys-Swart for typing the manuscript.—This study was made possible by a grant from the World Health Organization and by the Bureau of Foreign Affairs of the Free University.
Rights and permissions
About this article
Cite this article
Zylstra, U. Histochemistry and Ultrastructure of the Epidermis and the Subepidermal Gland Cells of the Freshwater Snails Lymnaea stagnalis and Biomphalaria pfeifferi . Z.Zellforsch 130, 93–134 (1972). https://doi.org/10.1007/BF00306996
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00306996