Skip to main content
Log in

Water and solute transport by the Malpighian tubules of the stick insect, Carausius morosus

The normal ultrastructure of the type 1 cells

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

Summary

Structural features of the principal, urine-secreting cells (type 1 cells) of the Malpighian tubules of Carausius are de scribedquantitatively and discussed in relation to possible mechanisms of water and solute transport. Mitochondria are arranged in two bands of about equal volume near to the basal and apical surfaces, suggesting active processes occur at both surfaces. Basal infoldings and apical microvilli which greatly amplify the cell surface are probably primarily devices to increase the passive permeability of the tissue to solutes. They do not provide functionally significant standing-osmotic-gradients. The extensive endoplasmic reticulum is locally differentiated into several components and ramifies between the infoldings and along microvilli but probably is not an intracellular conduit for the majority of urinary constituents. Vesicles and stages in their formation or liberation are observed both basally and apically although they probably do not contribute significantly to transcellular transport. At present it remains a problem to satisfactorily account for observations that the urine of Carausius can be hypotonic.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson, E. A., Harvey, W. R.: Active transport by the Cecropia midgut. II. Fine structure of the midgut epithelium. J. Cell Biol. 31, 107–134 (1966).

    Google Scholar 

  • Ashhurst, D. E.: The connective tissues of insects. Ann. Rev Ent. 13, 45–74 (1968).

    Google Scholar 

  • Baccetti, B., Mazzi, V., Massimello, G.: Ricerche istochimiche e al microscopio elettronico sui tubi Malpighiani di Dacus oleae, Gmel. II. L'adulto. Redia 48, 47–68 (1963).

    Google Scholar 

  • Beams, H. W., Tahmisian, T. N., Devine, R. L.: Electron microscope studies on the cells of the Malpighian tubules of the grasshopper, Melanoplus differentialis (Orthoptera, Acrididae) J. biophys. biochem. Cytol. 1, 197–202 (1955).

    Google Scholar 

  • Berkaloff, A.: Variations de l'ultrastructure des tubes de Malpighi et leur fonctionnement chez Gryllus domesticus (Orthoptère, Gryllidae). C. R. Acad. Sci. (Paris) 248, 466–469 (1959).

    Google Scholar 

  • —: Contribution à l'étude des tubes de Malpighi et de l'excrétion chez les insects. Observations au microscope électronique. Annls Sci. Nat. Zool., XII Ser. 2, 869–947 (1960).

    Google Scholar 

  • Berridge, M. J.: The physiology of excretion in the cotton stainer, Dysdercus fasciatus, Signoret. III. Nitrogen excretion and excretory metabolism. J. exp. Biol. 43, 535–552 (1965).

    Google Scholar 

  • —: The physiology of excretion in the cotton stainer, Dysdercus fasciatus, Signoret. IV. Hormonal control of excretion. J. exp. Biol. 44, 553–566 (1966).

    Google Scholar 

  • —: Urine formation by the Malpighian tubules of Calliphora. I. Cations. J. exp. Biol. 48, 159–174 (1968).

    Google Scholar 

  • —: Urine formation by the Malpighian tubules of Calliphora. II. Anions. J. exp. Biol. 50, 15–28 (1969).

    Google Scholar 

  • —, Oschman, J. L.: A structural basis for fluid secretion by Malpighian tubules. Tissue and Cell 1, 247–272 (1969).

    Google Scholar 

  • Bowers, B., Korn, E. D.: The fine structure of Acanthamoeba castellanii. I. The trophozoite. J. Cell Biol. 39, 95–111 (1968).

    Google Scholar 

  • Bruns, R. R., Palade, G. E.: Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries. J. Cell Biol. 37, 277–299 (1968).

    Google Scholar 

  • Bullivant, S., Loewenstein, W. R.: Structure of coupled and uncoupled cell junctions. J. Cell Biol. 37, 621–632 (1968).

    Google Scholar 

  • Bursell, E.: The excretion of nitrogen in insects. Adv. Insect Physiol. 4, 33–67 (1967).

    Google Scholar 

  • Craig, R.: The physiology of excretion in the insect. Ann. Rev. Ent. 5, 53–68 (1960).

    Google Scholar 

  • Crossley, A. C., Waterhouse, D. F.: The ultrastructure of a pheromone-secreting gland in the male scorpion fly, Harpobittacus australis (Bittacidae: Mecoptera). Tissue and Cell 1, 273–294 (1969).

    Google Scholar 

  • Dainty, J., House, C. R.: An examination of the evidence for membrane pores in the frog skin. J. Physiol. (Lond.) 185, 172–184 (1966).

    Google Scholar 

  • Davson, H.: A textbook of general physiology, 3rd ed. London: J. & A. Churchill Ltd. 1964.

    Google Scholar 

  • De Duve, C.: The lysosome. Scient. Am. 208, 64–72 (1963).

    Google Scholar 

  • Diamond, J. M.: The mechanism of water transport by the gall bladder. J. Physiol. (Lond.) 161, 503–527 (1962).

    Google Scholar 

  • —, Bossert, W. H.: Standing-gradient osmotic flow: a mechanism for coupling water and solute transport in epithelia. J. gen. Physiol. 50, 2061–2083 (1967).

    Google Scholar 

  • —: Functional consequencies of ultrastructural geometry in “backwards” fluid-transporting epithelia. J. Cell Biol. 37, 694–702 (1968).

    Google Scholar 

  • Diamond, J. M., Tormey, J. McD.: Role of long extracellular channels in fluid transport across epithelia. Nature (Lond.) 210, 817–820 (1966).

    Google Scholar 

  • Drochmans, P.: Morphologie du glycogène. Etude au microscope électronique de colorations négatives du glycogène particulaire. J. Ultrastruct. Res. 6, 141–163 (1962).

    Google Scholar 

  • Durbin, R., Frank, H., Solomon, A. K.: Water flow through frog gastric mucosa. J. gen. Physiol. 39, 535–551 (1956).

    Google Scholar 

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

    Google Scholar 

  • Fawcett, D. W.: Physiologically significant specialisations of the cell surface. Circulation 26, 1105–1125 (1962).

    Google Scholar 

  • Flower, N. E.: Frozen-etched septate junctions. Protoplasma (Wein) 70, 479–483 (1970).

    Google Scholar 

  • Graham, R. C., Karnovsky, M. J.: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291–302 (1966).

    Google Scholar 

  • Grimstone, A. V., Mullinger, A. M., Ramsay, J. A.: Further studies on the rectal complex of the mealworm, Tenebrio molitor, L. (Coleoptera, Tenebrionidae). Phil. Trans. B 253, 343–382 (1968).

    Google Scholar 

  • Hall, J. D., Crane, F. L.: An intracristal structure in beef heart mitochondria. Exp. Cell. Res. 62, 480–483 (1970).

    Google Scholar 

  • Hruban, Z., Rechcigl, M. Jr.: Microbodies and related particles. Morphology, biochemistry and physiology. Int. Rev. Cytol., Suppl. 1 (1969).

  • Irvine, H. B.: Sodium and potassium secretion by isolated insect Malpighian tubules. Amer. J. Physiol. 217, 1520–1527 (1969).

    Google Scholar 

  • Karnovsky, M. J.: Ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967).

    Google Scholar 

  • Kedem, O.: Water flow in the presence of active transport. Symp. Soc. exp. Biol. 19, 61–73 (1965).

    Google Scholar 

  • Kessel, R. G.: The permeability of dragon-fly Malpighian tubule cells to protein using horseradish peroxidase as a tracer. J. Cell Biol. 47, 299–303 (1970).

    Google Scholar 

  • Lane, N. J., Treherne, J. E.: Lanthanum staining of neurotubules in axons from cockroach ganglia. J. Cell Sci. 7, 217–231 (1970).

    Google Scholar 

  • Ledbetter, M. C., Porter, K. R.: A microtubule in plant cell fine structure. J. Cell Biol. 19, 239–250 (1963).

    Google Scholar 

  • Locke, M.: The structure of septate desmosomes. J. Cell Biol. 25, 166–169 (1965).

    Google Scholar 

  • —: The ultrastructure of the oenocytes in the moult/intermoult cycle of an insect. Tissue and Cell 1, 103–154 (1969).

    Google Scholar 

  • —, Collins, J. V.: Protein uptake in multivesicular bodies in the moult/intermoult cycle of an insect. Science 155, 467–469 (1967).

    Google Scholar 

  • Loewenstein, W. R., Kanno, Y.: Studies on an epithelial (gland) cell junction. I. Modification of surface membrane permeability. J. Cell Biol. 22, 565–586 (1964).

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Macgregor, H. C., Mackie, J. B.: Fine structure of the cytoplasm in salivary glands of Simulium. J. Cell Sci. 2, 137–144 (1967).

    Google Scholar 

  • Machen, T. E., Diamond, J. M.: An estimation of the salt concentration in the lateral intercellular spaces of rabbit gall bladder during maximal fluid transport. J. Membrane Biol. 1, 194–213 (1969).

    Google Scholar 

  • Maddrell, S. H. P.: Secretion by the Malpighian tubules of Rhodnius. The movements of ions and water. J. exp. Biol. 51, 71–97 (1969).

    Google Scholar 

  • - Fluid secretion by the Malpighian tubules of insects. Proc. roy. Soc. B (in press). (1971).

  • Mast, S. O., Fowler, C.: Permeability of Amoeba proteus to water, J. cell. comp. Physiol. 6, 151–167 (1935).

    Google Scholar 

  • Mercer, E. H., Brunet, P. C.: The electron microscopy of the left colleterial gland of the cockroach. J. biophys. biochem. Cytol. 5, 257–262 (1959).

    Google Scholar 

  • Meyer, G. F.: Elektronenmikroskopische Untersuchungen an den Malpighigefäßen verschiedener Insekten. Z. Zellforsch. 47, 18–28 (1957).

    Google Scholar 

  • Miller, F., Palade, G. E.: Lytic activities in renal protein absorption droplets. An electron microscopical cytochemical study. J. Cell Biol. 23, 519–552 (1964).

    Google Scholar 

  • Millonig, G.: Advantages of phosphate buffer for OsO4 solutions in fixation. J. appl. Phys. 32, 1637 (1961).

    Google Scholar 

  • —, Marinozzi, V.: Fixation and embedding in electron microscopy. Adv. optical electron Microscop. 2, 251–341 (1968).

    Google Scholar 

  • Moore, D. M., Ruska, H.: The fine structure of capillaries and small arteries. J. biophys. biochem. Cytol. 3, 457–462 (1957).

    Google Scholar 

  • Newcomb, E. H., Steer, M. W., Hepler, P. K., Wergin, W. P.: An atypical crista resembling a tight junction in bean root mitochondria. J. Cell Biol. 39, 35–42 (1968).

    Google Scholar 

  • Nicholls, J. G., Kuffler, S. W.: Extracellular space as a pathway for exchange between blood and neurons in the central nervous system of the leech: ionic composition of glial cells and neurons. J. Neurophysiol. 27, 645–671 (1964).

    Google Scholar 

  • Pappenheimer, J. R.: Passage of molecules through capillary walls. Physiol. Rev. 33, 387–423 (1953).

    Google Scholar 

  • Peachey, L. D.: Thin sections. 1. A study of section thickness and physical distortion produced during microtomy. J. biophys. biochem. Cytol. 4, 233–242 (1958).

    Google Scholar 

  • Pease, D. C.: Infolded basal plasma membranes found in epithelia noted for their water transport. J. biophys. biochem. Cytol. 2 (Suppl.), 203–208 (1956).

    Google Scholar 

  • Philpott, C. W., Copeland, D. E.: Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18, 389–404 (1963).

    Google Scholar 

  • Pilcher, D. E. M.: Hormonal control of the Malpighian tubules of the stick insect., Carausius morosus. J. exp. Biol. 52, 653–665 (1970a).

    Google Scholar 

  • —: The influence of diuretic hormone on the process of urine secretion by the Malpighian tubules of Carausius morosus. J. exp. Biol. 53, 465–484 (1970b).

    Google Scholar 

  • Ramsay, J. A.: The excretion of sodium and potassium by the Malpighian tubules of Rhodnius. J. exp. Biol. 29, 110–126 (1952).

    Google Scholar 

  • —: Active transport of potassium by the Malpighian tubules of insects. J. exp. Biol. 30, 358–369 (1963).

    Google Scholar 

  • —: Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 31, 104–113 (1954).

    Google Scholar 

  • —: The excretory system of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 32, 183–199 (1955a).

    Google Scholar 

  • —: The excretion of sodium, potassium and water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 32, 200–216 (1955b).

    Google Scholar 

  • —: Excretion by the Malpighian tubules of the stick insect (Orthoptera, Phasmidae): calcium, magnesium, chloride, phosphate and hydrogen ions. J. exp. Biol. 33, 697–708 (1956).

    Google Scholar 

  • —: Excretion by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae): amino acids, sugars and urea. J. exp. Biol. 35, 871–891 (1958).

    Google Scholar 

  • —: The rectal complex of the mealworm, Tenebrio molitor, L (Coleoptera, Tenebrionidae). Phil. Trans. B 248, 279–314 (1964).

    Google Scholar 

  • —, Brown, R. H. J.: Simplified apparatus and procedure for freezing point determinations upon small volumes fo fluid. J. sci. Instrum. 32, 372–375 (1955).

    Google Scholar 

  • Revel, J. P.: Electron microscopy of glycogen. J. Histochem. Cytochem. 12, 104–114 (1964).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Riegel, J. A.: Micropuncture studies of formed-body secretion by the excretory organs of crayfish, frog and stick insect. J. exp. Biol. 44, 379–385 (1966a).

    Google Scholar 

  • —: Analysis of formed bodies in urine removed from crayfish antennal gland by micropuncture. J. exp. Biol. 44, 387–395 (1966b).

    Google Scholar 

  • Rosenbluth, J.: Subsurface cisternae and their relationship to the neuronal plasmalemma. J. Cell Biol. 13, 405–421 (1962).

    Google Scholar 

  • Savage, A. A.: The development of the Malpighian tubules of Carausius morosus (Orthoptera). Quart. J. micr. Sci. 103, 417–437 (1962).

    Google Scholar 

  • Schneeburger-Keeley, E. E., Karnovsky, M. J.: The ultrastructural basis of alveolar-capillary membrane permeability to peroxidase used as a tracer. J. Cell Biol. 37, 781–793 (1968).

    Google Scholar 

  • Sedar, A. W.: Fine structure of the stimulated oxyntic cell. Fed. Proc. 24, 1360–1367 (1965).

    Google Scholar 

  • Smith, D. S.: Insect cells: their structure and function. Edinburgh and London: Oliver and Boyd 1968.

    Google Scholar 

  • Staubesand, J.: Cytopempsis. In: Funktionelle und morphologische Organisation der Zelle. II. Sekretion and Exkretion, S. 162–189. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • Stein, G.: Über den Feinbau der Duftdrüsen von Feuerwanzen (Pyrrhocoris aptercus, L., Geocorisae). Die 2. larvale Abdominaldrüse. Z. Zellforsch. 79, 49–63 (1967).

    Google Scholar 

  • Taylor, H. H.: Ultrastructural studies on the Malpighian tubules of the stick insect. Ph.D. Thesis, University of Newcastle upon Tyne (1970).

  • Tormey, J. McD., Diamond, J. M.: The ultrastructural route of fluid transport in rabbit gall bladder. J. gen. Physiol. 50, 2031–2060 (1967).

    Google Scholar 

  • Trump, B. F., Ericcson, J. L. E.: The effect of fixative solutions on the ultrastructure of cells and tissues. A comparative analysis with particular attention to the proximal convoluted tubule of the rat kidney. Lab. Invest. 14, 1245–1323 (1965).

    Google Scholar 

  • Wall, B. J.: Effects of dehydration and rehydration on the cockroach. J. Insect Physiol. 16, 1027–1042 (1970).

    Google Scholar 

  • Weibel, E. R., Kistler, G. S., Scherle, W. F.: Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38 (1966).

    Google Scholar 

  • Wessing, A.: Elektronenmikroskopische Studien zur Funktion der Malpighischen Gefäße von Drosophila melanogaster. I. Die Gefäße der Larve und Imago. Protoplasma (Wein) 55, 264–293 (1962).

    Google Scholar 

  • —: Elektronenmikroskopische Untersuchungen über die transzellulären Stoffbewegungen bei der Primärharnbildung der Insekten. Zool. Anz., Suppl. 27, 549–562 (1964).

    Google Scholar 

  • —: Die Funktion der Malpighischen Gefäße. In: Funktionelle und morphologische Organisation der Zelle. II. Sekretion und Exkretion, S. 228–268. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • —, Danneel, R.: Die Speicherung von Oxykynurenin in den Malpighischen Gefäßen verschiedener Augenfarbenmutaten von Drosophila melanogaster. Z. Naturforsch. 16b, 388–390 (1961).

    Google Scholar 

  • Whittembury, G., Oken, D. E., Windhager, D. E., Solomon, A. K.: Single proximal tubules of Necturus kidney. IV. Dependence of water movement on osmotic gradients. Amer. J. Physiol. 197, 1121–1127 (1959).

    Google Scholar 

  • Wigglesworth, V. B.: The storage of protein, fat, glycogen and uric acid in the fat body and other tissues of mosquito larvae. J. exp. Biol. 19, 56–77 (1942).

    Google Scholar 

  • —: The principles of insect physiology, 6th ed. London: Methuen and Co. Ltd. 1965.

    Google Scholar 

  • —, Salpeter, M. M.: Histology of the Malpighian tubules in Rhodnius prolixus, Stål (Hemiptera) J. Insect Physiol. 8, 299–307 (1962).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This investigation formed part of a dissertation for the degree of Ph. D. in the University of Newcastle upon Tyne. It is a pleasure to thank Prof. J. Shaw for his advice and encouragement and the Science Research Council for financial support.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taylor, H.H. Water and solute transport by the Malpighian tubules of the stick insect, Carausius morosus . Z. Zellforsch. 118, 333–368 (1971). https://doi.org/10.1007/BF00331192

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00331192

Key-Words

Navigation