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.
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).
Ashhurst, D. E.: The connective tissues of insects. Ann. Rev Ent. 13, 45–74 (1968).
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).
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).
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).
—: 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).
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).
—: The physiology of excretion in the cotton stainer, Dysdercus fasciatus, Signoret. IV. Hormonal control of excretion. J. exp. Biol. 44, 553–566 (1966).
—: Urine formation by the Malpighian tubules of Calliphora. I. Cations. J. exp. Biol. 48, 159–174 (1968).
—: Urine formation by the Malpighian tubules of Calliphora. II. Anions. J. exp. Biol. 50, 15–28 (1969).
—, Oschman, J. L.: A structural basis for fluid secretion by Malpighian tubules. Tissue and Cell 1, 247–272 (1969).
Bowers, B., Korn, E. D.: The fine structure of Acanthamoeba castellanii. I. The trophozoite. J. Cell Biol. 39, 95–111 (1968).
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).
Bullivant, S., Loewenstein, W. R.: Structure of coupled and uncoupled cell junctions. J. Cell Biol. 37, 621–632 (1968).
Bursell, E.: The excretion of nitrogen in insects. Adv. Insect Physiol. 4, 33–67 (1967).
Craig, R.: The physiology of excretion in the insect. Ann. Rev. Ent. 5, 53–68 (1960).
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).
Dainty, J., House, C. R.: An examination of the evidence for membrane pores in the frog skin. J. Physiol. (Lond.) 185, 172–184 (1966).
Davson, H.: A textbook of general physiology, 3rd ed. London: J. & A. Churchill Ltd. 1964.
De Duve, C.: The lysosome. Scient. Am. 208, 64–72 (1963).
Diamond, J. M.: The mechanism of water transport by the gall bladder. J. Physiol. (Lond.) 161, 503–527 (1962).
—, Bossert, W. H.: Standing-gradient osmotic flow: a mechanism for coupling water and solute transport in epithelia. J. gen. Physiol. 50, 2061–2083 (1967).
—: Functional consequencies of ultrastructural geometry in “backwards” fluid-transporting epithelia. J. Cell Biol. 37, 694–702 (1968).
Diamond, J. M., Tormey, J. McD.: Role of long extracellular channels in fluid transport across epithelia. Nature (Lond.) 210, 817–820 (1966).
Drochmans, P.: Morphologie du glycogène. Etude au microscope électronique de colorations négatives du glycogène particulaire. J. Ultrastruct. Res. 6, 141–163 (1962).
Durbin, R., Frank, H., Solomon, A. K.: Water flow through frog gastric mucosa. J. gen. Physiol. 39, 535–551 (1956).
Farquhar, M. G., Palade, G. E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).
Fawcett, D. W.: Physiologically significant specialisations of the cell surface. Circulation 26, 1105–1125 (1962).
Flower, N. E.: Frozen-etched septate junctions. Protoplasma (Wein) 70, 479–483 (1970).
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).
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).
Hall, J. D., Crane, F. L.: An intracristal structure in beef heart mitochondria. Exp. Cell. Res. 62, 480–483 (1970).
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).
Karnovsky, M. J.: Ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967).
Kedem, O.: Water flow in the presence of active transport. Symp. Soc. exp. Biol. 19, 61–73 (1965).
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).
Lane, N. J., Treherne, J. E.: Lanthanum staining of neurotubules in axons from cockroach ganglia. J. Cell Sci. 7, 217–231 (1970).
Ledbetter, M. C., Porter, K. R.: A microtubule in plant cell fine structure. J. Cell Biol. 19, 239–250 (1963).
Locke, M.: The structure of septate desmosomes. J. Cell Biol. 25, 166–169 (1965).
—: The ultrastructure of the oenocytes in the moult/intermoult cycle of an insect. Tissue and Cell 1, 103–154 (1969).
—, Collins, J. V.: Protein uptake in multivesicular bodies in the moult/intermoult cycle of an insect. Science 155, 467–469 (1967).
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).
Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Macgregor, H. C., Mackie, J. B.: Fine structure of the cytoplasm in salivary glands of Simulium. J. Cell Sci. 2, 137–144 (1967).
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).
Maddrell, S. H. P.: Secretion by the Malpighian tubules of Rhodnius. The movements of ions and water. J. exp. Biol. 51, 71–97 (1969).
- 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).
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).
Meyer, G. F.: Elektronenmikroskopische Untersuchungen an den Malpighigefäßen verschiedener Insekten. Z. Zellforsch. 47, 18–28 (1957).
Miller, F., Palade, G. E.: Lytic activities in renal protein absorption droplets. An electron microscopical cytochemical study. J. Cell Biol. 23, 519–552 (1964).
Millonig, G.: Advantages of phosphate buffer for OsO4 solutions in fixation. J. appl. Phys. 32, 1637 (1961).
—, Marinozzi, V.: Fixation and embedding in electron microscopy. Adv. optical electron Microscop. 2, 251–341 (1968).
Moore, D. M., Ruska, H.: The fine structure of capillaries and small arteries. J. biophys. biochem. Cytol. 3, 457–462 (1957).
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).
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).
Pappenheimer, J. R.: Passage of molecules through capillary walls. Physiol. Rev. 33, 387–423 (1953).
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).
Pease, D. C.: Infolded basal plasma membranes found in epithelia noted for their water transport. J. biophys. biochem. Cytol. 2 (Suppl.), 203–208 (1956).
Philpott, C. W., Copeland, D. E.: Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18, 389–404 (1963).
Pilcher, D. E. M.: Hormonal control of the Malpighian tubules of the stick insect., Carausius morosus. J. exp. Biol. 52, 653–665 (1970a).
—: 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).
Ramsay, J. A.: The excretion of sodium and potassium by the Malpighian tubules of Rhodnius. J. exp. Biol. 29, 110–126 (1952).
—: Active transport of potassium by the Malpighian tubules of insects. J. exp. Biol. 30, 358–369 (1963).
—: Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 31, 104–113 (1954).
—: The excretory system of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 32, 183–199 (1955a).
—: 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).
—: 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).
—: 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).
—: The rectal complex of the mealworm, Tenebrio molitor, L (Coleoptera, Tenebrionidae). Phil. Trans. B 248, 279–314 (1964).
—, Brown, R. H. J.: Simplified apparatus and procedure for freezing point determinations upon small volumes fo fluid. J. sci. Instrum. 32, 372–375 (1955).
Revel, J. P.: Electron microscopy of glycogen. J. Histochem. Cytochem. 12, 104–114 (1964).
Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain. J. Cell Biol. 17, 208–212 (1963).
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).
—: Analysis of formed bodies in urine removed from crayfish antennal gland by micropuncture. J. exp. Biol. 44, 387–395 (1966b).
Rosenbluth, J.: Subsurface cisternae and their relationship to the neuronal plasmalemma. J. Cell Biol. 13, 405–421 (1962).
Savage, A. A.: The development of the Malpighian tubules of Carausius morosus (Orthoptera). Quart. J. micr. Sci. 103, 417–437 (1962).
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).
Sedar, A. W.: Fine structure of the stimulated oxyntic cell. Fed. Proc. 24, 1360–1367 (1965).
Smith, D. S.: Insect cells: their structure and function. Edinburgh and London: Oliver and Boyd 1968.
Staubesand, J.: Cytopempsis. In: Funktionelle und morphologische Organisation der Zelle. II. Sekretion and Exkretion, S. 162–189. Berlin-Heidelberg-New York: Springer 1965.
Stein, G.: Über den Feinbau der Duftdrüsen von Feuerwanzen (Pyrrhocoris aptercus, L., Geocorisae). Die 2. larvale Abdominaldrüse. Z. Zellforsch. 79, 49–63 (1967).
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).
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).
Wall, B. J.: Effects of dehydration and rehydration on the cockroach. J. Insect Physiol. 16, 1027–1042 (1970).
Weibel, E. R., Kistler, G. S., Scherle, W. F.: Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38 (1966).
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).
—: Elektronenmikroskopische Untersuchungen über die transzellulären Stoffbewegungen bei der Primärharnbildung der Insekten. Zool. Anz., Suppl. 27, 549–562 (1964).
—: 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.
—, Danneel, R.: Die Speicherung von Oxykynurenin in den Malpighischen Gefäßen verschiedener Augenfarbenmutaten von Drosophila melanogaster. Z. Naturforsch. 16b, 388–390 (1961).
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).
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).
—: The principles of insect physiology, 6th ed. London: Methuen and Co. Ltd. 1965.
—, Salpeter, M. M.: Histology of the Malpighian tubules in Rhodnius prolixus, Stål (Hemiptera) J. Insect Physiol. 8, 299–307 (1962).
Author information
Authors and Affiliations
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
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
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00331192