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Morphometric analysis of the midgut of female Aedes aegypti (L.) (insecta, diptera) under various physiological conditions

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Summary

The ultrastructure of the midgut of Aedes aegypti females was investigated by means of morphometric techniques. The interest was focussed on quantitative differences in the composition of epithelial cells between the anterior (A) and posterior (P) part of the midgut. The aim was to attribute defined functions to each of these 2 parts.

5 different physiological stages were compared: 1 = immature female; 2 = ready for first blood meal (b.m.); 3 = digestion of b.m.; 4 = ready for 2nd b.m.; 5 = aging female.

Whereas in stage 1, when the gut has not yet reached a functional state the epithelial cells of A and P resemble each other, distinct differences develop in subsequent stages. Generally the cell volume and the nuclear-cytoplasmic ratio become higher in P than in A. Concomitantly the mitochondrial content and the surface area of the rough endoplasmic reticulum are more prominent in P than in A. On the other hand more microvilli, a more extensive basal labyrinth and a well developed smooth endoplasmic reticulum are present in A.

Enlarged cytoplasmic volumes, especially high in P, are found 24 h after the first b.m. (stage 3). In accordance with this increase the volume of organelles and/or their membrane surface areas also reach maximal values. This augmentation of the metabolic cell apparatus suggests that during blood digestion the whole organ develops an increased functional capacity.

From the quantitative structural differences in A and P we concluded that the A-part of the midgut is especially involved in absorption. To the P-part more protein synthesis may be attributed, thus indicating an enhanced formation of digestive enzymes.

Although this study deals with a rather specialised insect (blood digestion), it appears that our hypothesis attributing functions to defined midgut zones, agrees to a certain extent with the “secretion-absorption-model” of Berridge (1970).

Zusammenfassung

Die Ultrastruktur des Mitteldarmes von Aedes aegypti Weibchen wurde morphometrisch untersucht. Besonderes Interesse lag dabei auf quantitativen Unterschieden im Bau der Epithelzellen eines vorderen (A) und eines hinteren (P) Abschnittes des Mitteldarmes, um jedem dieser beiden Abschnitte bestimmte Funktionen zuordnen zu können.

5 physiologisch verschiedene Stadien wurden verglichen: 1 = unreife Weibchen; 2 = zum 1. Blutmahl (B.M.) bereit; 3 = Verdauung des B.M.; 4 = zum 2. B.M. bereit; 5 = alternde Weibchen.

Wenn der Mitteldarm noch nicht funktionsbereit ist (Stadium 1) gleichen sich die Epithelzellen von A und P quantitativ ultrastrukturell. In den folgenden Stadien hingegen werden deutliche Unterschiede sichtbar. Das Zellvolumen und die Kern-Cytoplasma-Relation werden in P generell größer als in A. Parallel dazu nehmen der Mitochondriengehalt und die Oberfläche des rauhen endoplasmatischen Retikulums in P gegenüber A zu. In A entwickeln sich mehr Microvilli, ein extensiveres basales Labyrinth und ein deutliches glattes endoplasmatisches Retikulum.

Vergrößerte Cytoplasmavolumina vor allem in den P-Zellen werden 24 Std. nach dem 1. B.M. gefunden (Stadium 3). Parallel dazu erreichen die Volumina der Organellen und/oder ihre Membranoberflächen ebenfalls Maximalwerte. Diese Vergrößerung des gesamten Zell-apparates läßt den Schluß zu, daß während der Blutverdauung die Funktionskapazität des Mitteldarmes erhöht ist.

Basierend auf den quantitativ ultrastrukturellen Unterschieden zwischen den Zellen von A und P wurde postuliert, daß dem vorderen Abschnitt des Mitteldarms verstärkte Absorptionsfunktionen zukommen. Dem hinteren Abschnitt hingegen wurden gesteigerte Protein-syntheseleistungen im Zusammenhang mit der Bildung von Verdauungsenzymen zugeordnet.

Die vorliegenden Resultate wurden an einem, in Beziehung auf seine Ernährung, spezialisierten Insekt gewonnen (Blutverdauung). Trotzdem scheint die postulierte Zuordnung von Funktionen zu bestimmten Mitteldarmzonen mit dem “secretion—absorption”-Modell (Berridge, 1970) übereinzustimmen.

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References

  • Akov, S.: Inhibition of blood digestion and oocyte growth in Aedes aegypti by 5-Fluorouracil. Biol. Bull. mar. biol. Lab. Woods Hole 129, 439–453 (1965)

    Google Scholar 

  • Akov, S.: Retention of the blood-meal in Aedes aegypti following sterilization by chemicals and irradiation. Ann. trop. Med. Parasit. 60, 482–194 (1966)

    Google Scholar 

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

  • Briegel, H., Kaiser, C.: Life-span of mosquitoes under laboratory conditions. Gerontologia 19, 240–249 (1973)

    Google Scholar 

  • Christophers, R.: Aedes aegypti: The yellow fever mosquito: Its life history, bionomics and structure, 739 pp. Cambridge Univ. Press 1960

  • Clay, M. E., Venard, C. E.: The fine structure of the oesophageal diverticula in the mosquito Aedes triseriatus (Dipt. Cul.). Ann. entomol. Soc. Amer. 65, 964–975 (1972)

    Google Scholar 

  • Day, M. F.: The mechanism of food distribution to midgut or diverticula in the mosquito. Aust. J. biol. Sci. 7, 515–524 (1954)

    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 

  • Fisk, F. W.: Studies on proteolytic digestion in adult Aedes aegypti mosquitoes. Ann. entomol. Soc. Amer. 43, 555–572 (1950)

    Google Scholar 

  • Fisk, F. W., Shambaugh, G. F.: Protease activity in adult Aedes aegypti mosquitoes as related to feeding. Ohio J. Sci. 52, 80–88 (1952)

    Google Scholar 

  • Fisk, F. W., Shambaugh, G. F.: Invertase activity in adult Aedes aegypti mosquitoes. Ohio J. Sci. 54, 237–239 (1954)

    Google Scholar 

  • Freyvogel, T. A., Jaquet, C.: The prerequisites of the formation of a peritrophic membrane in Culicidae females. Acta trop. (Basel) 22, 148–154 (1965)

    Google Scholar 

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

    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 

  • Geering, K., Freyvogel, T. A.: The distribution of acetylcholine and unspecific esterases in the midgut lumen and epithelium of Aedes aegypti L. females. Comp. Biochem. Physiol. in press

  • Gooding, R. H.: Digestive processes of haematophagous insects I. A literature review. Quaestiones entomol. 8, 5–60 (1972)

    Google Scholar 

  • 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., 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 mosquitces. Canad. Entomol. 105, 433–436 (1973)

    Google Scholar 

  • Hagedorn, H. H., Judson, C. L.: Purification and site of synthesis of Aedes aegypti yolk proteins. J. exp. Zool. 182, 367–378 (1972)

    Google Scholar 

  • Hayes, R. O.: Determination of a physiological saline solution for Aedes aegypti L. J. econ. Entomol. 46, 624–627 (1953)

    Google Scholar 

  • Hecker, H., Bleiker, S.: Feinstruktur und Funktion des ventralen Darmdivertikels bei Aedes aegypti-Weibchen (Insecta, Diptera). Rev. suisse Zool. 79, 1028–1031 (1972)

    Google Scholar 

  • Hecker, H., Burri, P. H., Steiger, R., Geigy, R.: Morphometric data on the ultrastructure of pleomorphic bloodforms of Trypanosoma brucei, Plimmer & Bradford, 1899. Acta trop. (Basel) 29, 182–198 (1972)

    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 (1971a)

    Google Scholar 

  • Hecker, H., Freyvogel, T. A., Briegel, H., Steiger, R.: The ultrastructure of midgut epithelium in Aedes aegypti L. (Insecta, Diptera) males. Acta trop. (Basel) 28, 275–290 (1971b)

    Google Scholar 

  • Jones, J. C., Zeve, V. H.: The fine structure of gastric caeca of Aedes aegypti larvae. J. Insect Physiol. 14, 1567–1575 (1968)

    Google Scholar 

  • Meredith, J., Phillips, J. E.: Ultrastructure of the anal papillae of a salt-water mosquito larva, Aedes campestris. J. Insect Physiol. 19, 1157–1172 (1973)

    Google Scholar 

  • Noirot, Ch., Noirot-Timothée, C.: Structure fine de la bordure en brosse de l'intestin moyen chez les insectes. J. de Microscopie 13, 85–87 (1972)

    Google Scholar 

  • Plattner, H.: Quantitative Struktur-Funktions-Korrelation an Biomembranen. Progr. Histochem. Cytochem. 5, 3 (1973)

    Google Scholar 

  • Priester, W. de: Ultrastructure of the midgut epithelial cells in the fly, Calliphora erythrocephala. J. Ultrastruct. Res. 36, 783–805 (1971)

    Google Scholar 

  • Priester, W. de: Lysosomes in the midgut of Calliphora erythrocephala Meigen. Z. Zellforsch. 129, 430–446 (1972)

    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 

  • Richards, A. G., Richards, P. A.: Origin and composition of the peritrophic membrane of the mosquito, Aedes aegypti. J. Insect Physiol. 17, 2253–2275 (1971)

    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 

  • Riley, J.: Histochemical and ultrastructural observations on digestion in Tetrameres fissispina Diesing, 1891 (Nematoda: Spiruridea) with special reference to intracellular digestion. Int. J. Parasit. 3, 157–164 (1973)

    Google Scholar 

  • Roth, T. F., Porter, K.: Yolk protein uptake in the oocyte of the mosquito Aedes aegypti L. J. Cell Biol. 20, 313–332 (1964)

    Google Scholar 

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

    Google Scholar 

  • Stohler, H.: Analyse des Infektionsverlaufes von Plasmodium gallinaceum im Darm von Aedes aegypti. Acta trop. (Basel) 14, 302–352 (1957)

    Google Scholar 

  • Thayer, D. W., Terzian, L. A., Price, P. A.: Digestion of the human blood-meal by the mosquito Aedes aegypti. J. Insect Physiol. 17, 2469–2473 (1971)

    Google Scholar 

  • Treherne, J. E.: Gut absorption (Review). Ann. Rev. Entomol. (1967)

  • Wagner, C., Tenorio, P. A., Terzian, L. A.: A study of two proteolytic enzymes from mosquito tissue. Research report No. 6, Naval Medical Research Institute Bethesda, Maryland (1961)

    Google Scholar 

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

    Google Scholar 

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Authors and Affiliations

  1. Swiss Tropical Institute, Basle, Switzerland

    Hermann Hecker, Reto Brun & Christoph Reinhardt

  2. Department of Anatomy, Berne, Switzerland

    Peter H. Burri

Authors
  1. Hermann Hecker
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  2. Reto Brun
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  3. Christoph Reinhardt
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  4. Peter H. Burri
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Additional information

This work has partly been supported by the “Schweizerischer Nationalfonds zur Förderung der wissenschaftlichen Forschung”. The authors are indebted to Prof. T. A. Freyvogel and Prof. E. R. Weibel for their interest in this study and for their valuable discussions. The excellent technical assistance of Miss Silvia Bleiker is greatly acknowledged. We would like to thank the laboratory of Dr. K. Geering and especially Miss J. Watts for providing us with mosquitoes, as well as Miss V. Schmutz and Miss E. Zehnder for typing the manuscript.

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Hecker, H., Brun, R., Reinhardt, C. et al. Morphometric analysis of the midgut of female Aedes aegypti (L.) (insecta, diptera) under various physiological conditions. Cell Tissue Res. 152, 31–49 (1974). https://doi.org/10.1007/BF00224209

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