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Structure and function of midgut epithelial cells in culicidae mosquitoes (insecta, diptera)

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Summary

The midgut of female Anophelinae and Culicinae comprises a narrow anterior (A-part) and a wide posterior part (P-part, stomach). Both are lined by a singlelayered epithelium, and in both parts regenerative cells are found between the epithelial cells. “Clear cells”, possibly with an endocrine function, are only found in the P-part.

The epithelial cells of the mosquito species investigated display close ultrastructural similarities. No significant differences are found between Anopheles gambiae and A. stephensi which differ markedly in origin and habitat.

In all species investigated the cellular organization suggests that both midgut parts are able to carry out processes of synthesis and secretion as well as of absorption and transport. On the other hand, in the A-part more microvilli, a higher density of membranes of the smooth endoplasmic reticulum and a tendency for more membranes of the basal labyrinth are seen by comparison with the P-part. The P-part is characterized by more rough endoplasmic reticulum (rer) and mitochondria.

As a working hypothesis it is proposed that absorption of sugar-containing solutions and the formation of mucus-like material occurs in A. The P-part is postulated to be responsible for synthesis and release of precursors of the peritrophic membrane and digestive enzymes as well as for the main absorption, transport and temporary storage of metabolites resulting from blood digestion.

Ultrastructural differences between mosquito species mainly consist of the following:

  1. a)

    less surface density of rer in the P-part of Culex and Anopheles as compared with Aedes; more rer in P than in A of Anopheles only present from 1st blood meal onwards,

  2. b)

    an additional rer cisterna in Culex forms a “halo” around the nucleus,

  3. c)

    apical granules in the P-part of Anopheles,

  4. d)

    storage deposits — in Aedes primarily as lipids — in Anopheles as carbohydrates and lipids,

  5. e)

    no maculae adhaerentes in the P-part of Anopheles.

Zusammenfassung

Der Mitteldarm der untersuchten Anophelinae und Culicinae-Weibchen ist in einen engen vordem (A-part) und in einen weiten hintern Abschnitt (P-part, Magen) gegliedert. Das Epithel ist einschichtig. Regenerationszellen findet man im A- und P-part. “Helle Zellen” (“clear cells”) mit möglicherweise endokriner Funktion kommen lediglich im P-part vor.

In vielen strukturellen Parametern gleichen sich die Epithelzellen der verschiedenen Mückenarten. Keine wesentlichen Unterschiede bestehen zwischen Anopheles gambiae (“Wildfänge”) und A. stephensi (Laborstamm).

Die Zellstruktur läßt vermuten, daß in beiden Mitteldarmabschnitten sowohl Synthese und Sekretionsvorgänge als auch Resorptionsund Transportprozesse ablaufen können. Daneben enthält der A-part mehr Mikrovilli, einen größeren Anteil an glattem endoplasmatischem Retikulum und an Membranen des basalen Labyrinths. Der P-part ist gekennzeichnet durch einen höheren Anteil an rauhem endoplasmatischem Retikulum (rer) und an Mitochondrien.

Als Arbeitshypothese wurde dem A-part aller untersuchten Culiciden die Bildung und Sekretion von Mucus-ähnlichen Substanzen und die Resorption von Zucker zugeordnet. Dementsprechend sollte im P-part sowohl Synthese und Sekretion der peritrophen Membran und der Enzyme für die Blutverdauung als auch zu wesentlichen Teilen Resorption, Transport und temporäre Speicherung von Blutabbauprodukten stattfinden.

Strukturelle Unterschiede zwischen den untersuchten Mückenarten bestehen zur Hauptsache im Folgenden:

  1. a)

    weniger Oberflächendichte des rer im P-part von Culex und Anopheles verglichen mit Aedes; erst während und nach der Verdauung des 1. Blutmahls mehr rer in P als in A,

  2. b)

    eine zusätzliche rer Cisterne bildet bei Culex einen “Kernhof”,

  3. c)

    apicale Granula im P-part von Anopheles,

  4. d)

    Reserveprodukte bei Aedes als Lipide gespeichert, bei Anopheles als Kohlenhydrate und Lipide,

  5. e)

    keine Maculae adhaerentes im P-part von Anopheles.

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References

  • Bauer, P., Rudin, W., Hecker, H.: Ultrastructural changes in midgut cells of female Aedes aegypti L. (Insecta, Diptera) after starvation or sugar diet. Cell Tiss. Res. 177, 215–219 (1977)

    Google Scholar 

  • Berridge, M.J.: A structural analysis of intestinal absorption. In: Insect ultrastructure, ed. by A.C. Neville, pp. 135–151. Oxford & Edinburgh: Blackwell Scientific Publ. 1970

    Google Scholar 

  • Bertram, D.S., Bird, R.G.: Studies on mosquito-borne viruses in their vectors. I. The normal fine structure of the midgut epithelium of the adult female Aedes aegypti L. and the functional significance of its modification following a blood meal. Trans. roy. Soc. trop. Med. Hyg. 55, 404–423 (1961)

    Google Scholar 

  • Böhringer, S.: Digestion in the tsetse fly: An ultrastructural analysis of structure and function of the midgut epithelium in Glossina morsitans morsitans (Machado), (Diptera: Glossinidae). In preparation

  • Bonnanfant-Jais, M.L.: Morphologie de la glande lactée d'une glossine, Glossina austeni Newst, au cours du cycle de gestation. II. Aspects ultrastructuraux en période de repos et au cours des gestations successives. J. Microscopie 24, 295–314 (1975)

    Google Scholar 

  • Ericsson, J.L.E., Trump, B.F.: Observations on the application of electron microscopy of the lead phosphate technique for the demonstration of acid phosphatase. Histochemie 4, 470–487 (1964–1965)

    Google Scholar 

  • Fawcett, D.W.: An atlas of fine structure: The cell, its organelles and inclusions, 448 pp. Philadelphia and London: W.B. Saunders Comp. 1966

    Google Scholar 

  • Freyvogel, T.A., Stäubli, W.: The formation of the peritrophic membrane in Culicidae. Acta trop. (Basel) 22, 118–147 (1965)

    Google Scholar 

  • Fuchs, M.S., Fong, W.F.: Inhibition of blood digestion by α-amanitin and actinomycin D and its effect on ovarian development in Aedes aegypti. J. Insect Physiol. 22, 465–472 (1976)

    Google Scholar 

  • Gander, E.: Zur Histologie und Histochemie des Mitteldarmes von Aedes aegypti und Anopheles stephensi in Zusammenhang mit der Blutverdauung. Acta trop. (Basel) 25, 133–175 (1968)

    Google Scholar 

  • Gass, R.: Einfluß der Blutverdauung auf die Entwicklung von Plasmodium gallinaceum (Brumpt) im Mitteldarm von Aedes aegypti L. Ph.D. Dissertation. Univ. Basel (1977)

  • Geigy, R., Herbig, A. Erreger und Überträger tropischer Krankheiten. Acta trop. (Basel), Suppl. 6, 472pp. 1955

  • Gooding, R.H.: The digestive processes of haematophagous insects. IV. Secretion of trypsin by Aedes aegypti (Diptera: Culicidae). Canad. Entomol. 105, 599–603 (1973)

    Google Scholar 

  • Gooding, R.H.: Digestive enzymes and their control in haematophagous arthropods. Acta trop. (Basel) 32, 96–111 (1975)

    Google Scholar 

  • Gooding, R.H., Cheung, A.C., Rolseth, B.M.: The digestive processes of haematophagous insects. III. Inhibition of trypsin by honey and the possible functions of the oesophageal diverticula of mosquitoes. Canad. Entomol. 105, 433–436 (1973)

    Google Scholar 

  • Hecker, H., Brun, R.: Morphometric differences in midgut epithelial cells between strains of female Aedes aegypti (L.) (Insecta, Diptera). Cell Tiss. Res. 159, 91–99 (1975)

    Google Scholar 

  • Hecker, H., Brun, R., Reinhardt, C., Burri, P.H.: Morphomeric analysis of the midgut of female Aedes aegypti L. (Insecta, Diptera) under various physiological conditions. Cell Tiss. Res. 152, 31–49 (1974)

    Google Scholar 

  • Hecker, H., Freyvogel, T.A., Briegel, H., Steiger, R.: Ultrastructural differentiation of the midgut epithelium in female Aedes aegypti L. (Insecta, Diptera) imagines. Acta trop. (Basel) 28, 80–104 (1971)

    Google Scholar 

  • Hecker, H., Rudin, W.: The midgut of Aedes aegypti L. (Insecta, Diptera) during blood digestion. In preparation

  • Jenni, L.: Synthese und Aufnahme von Proteinen während der Vitellogenese in Ovocyten von Ornithodorus moubata, Murray (Ixodoidae, Argasidae). Acta trop. (Basel) 28, 105–163 (1971)

    Google Scholar 

  • Jenni, L., Boehringer, S.: Nuclear coat and viruslike particles in the midgut epithelium of Glossina morsitans sspp. Acta trop. (Basel) 33, 380–389 (1976)

    Google Scholar 

  • Lehane, M.J.: Digestive enzyme secretion in Stomoxys calcitrans (Diptera, Muscidae). Cell Tiss. Res. 170, 275–287 (1976)

    Google Scholar 

  • Ramstein, H., Hecker, H.: Cellular changes in the midgut of Aedes aegypti L. (Insecta, Diptera) in the course of three bloodmeals. Unpublished

  • Reinhardt, C.: Ultrastructural comparison of the midgut epithelia of fleas with different feeding behavior patterns (Xenopsylla cheopis, Echidnophage gallinaceae, Tunga penetrans, Siphonaptera, Pulicidae). Acta trop. (Basel) 33, 105–132 (1976)

    Google Scholar 

  • Reinhardt, C., Hecker, H.: Structure and function of the basal lamina and of the cell junctions in the midgut epithelium (stomach) of female Aedes aegypti L. (Insecta, Diptera). Acta trop. (Basel) 30, 213–236 (1973)

    Google Scholar 

  • Richardson, M.W., Romoser, W.S.: The formation of the peritrophic membrane in adult Aedes triseriatus. J. med. Entomol. 9, 495–500 (1972)

    Google Scholar 

  • Rudin, W., Böhringer, S., Hecker, H.: Autoradiographic investigation of cellular functions in Aedes aegypti midgut. In preparation

  • Rudin, W., Hecker, H.: Morphometric comparison of the midgut epithelial cells in male and female Aedes aegypti L. (Insecta, Diptera). Tissue and Cell 8, 459–470 (1976)

    Google Scholar 

  • Russell, P.F., Rozeboom, L.E., Stone, A.: Keys to the Anopheline mosquitoes of the world, 152pp. Philadelphia: Amer. Ent. Soc., Acad. Nat. Sci. 1943

    Google Scholar 

  • Samish, M., Akov, S.: Influence of feeding on midgut protease activity in Aedes aegypti. Israel J. Entomol. 7, 41–48 (1972)

    Google Scholar 

  • Stäubli, W., Freyvogel, T.A., Suter, J.: Structural modifications of the endoplasmatic reticulum of midgut epithelial cells of mosquitoes in relation to blood intake. J. Microscopie 5, 189–204 (1966)

    Google Scholar 

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

    Google Scholar 

  • Vanderberg, J., Rhodin, J., Yoeli, M.: Electron microscopic and histochemical studies of sporozoite formation in Plasmodium berghei. J. Protozool. 14, 82–103 (1967)

    Google Scholar 

  • Weibel, E.R.: Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 26, 235–302 (1969)

    Google Scholar 

  • Weymarn, N. von, Rudin, W., Hecker, H.: Clear cells in the digestive tract of Aedes aegypti L. (Insecta, Diptera). In preparation

  • Wilcocks, C., Manson-Bahr, P.E.C.: Manson's tropical diseases, 1164 pp. London: Baillière Tindall 1972

    Google Scholar 

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I thank Prof. T.A. Freyvogel for his practical instructions in collecting, determining and breeding A. gambiae in Ifakara, Tanzania. The critical discussion of the manuscript by my collegues Drs. S. Böhringer, P.H. Burri and W. Rudin as well as English language corrections by Dr. R. Yeates and by the Copy-editor of “Cell and Tissue Research” are gratefully acknowledged. I thank Mr. P. Bauer for preparing the C.p.fatigans material, Miss C. Fauser for skillful technical assistance, and Miss U. Steffen for typing the manuscript

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Hecker, H. Structure and function of midgut epithelial cells in culicidae mosquitoes (insecta, diptera). Cell Tissue Res. 184, 321–341 (1977). https://doi.org/10.1007/BF00219894

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