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Morphological changes in the middle intestine of the rainbow trout, Salmo gairdneri, induced by a hyperosmotic environment

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Summary

The structural modifications in the middle intestine of the trout, Salmo gairdneri, induced by transfer to seawater have been studied. During the first two days in seawater, significant distensions of the intercellular spaces are observed between the apical tight junctions and the basement membrane. These dilations are more frequent in the apical part of the intestinal folds. At the basal part of the cell, numerous lamellar processes open in the intercellular spaces. They are closely associated with elongated mitochondria, and are often mixed with small clear vesicles. After seven days in seawater, intercellular spaces are less expanded. Numerous mitochondria are observed in the apical part of the cell, and numerous myelinic bodies with dense granules lie near the nucleus. After one month in seawater, the epithelium resembles that of the freshwater controls; mitochondria are more numerous and other organelles are well developed. The most important modifications of the ultrastructure of the intestine mucosa occur during the first two days in seawater, in correlation with important physiological changes following the abrupt increase of environmental salinity.

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References

  • Ball JN, Jones C, Forster ME, Margreaves G, Hawkins EF, Milne KP (1971) Measurement of plasma cortisol levels in the eel Anguilla anguilla in relation to osmotic adjustments. J Endocrinol 50:75–96

    Google Scholar 

  • Bath RN, Eddy FB (1979) Salt and water balance in rainbow trout (Salmo gairdneri) rapidly transferred from freshwater to sea water. J Exp Biol 83:193–202

    Google Scholar 

  • Bauermeister AE, Pirie BJS, Sargent JR (1979) An electron microscopic study of lipid absorption in the pyloric caeca of rainbow trout (Salmo gairdneri) fed wax ester-rich zooplancton. Cell Tissue Res 200:475–486

    Google Scholar 

  • Bentzel CJ, Parsa B, Hare DK (1969) Osmotic flow across proximal tubule of Necturus: Correlation of physiologic and anatomic studies. Am J Physiol 217, 2:570–580

    Google Scholar 

  • Bergot P, Flechon JE (1970a) Forme et voie d'absorption intestinale des acides gras à chaîne longue chez la Truite arc-en-ciel Salmo gairdneri R. I. Lipides en particules. Ann Biol Anim Biochim Biophys 10:459–472

    Google Scholar 

  • Bergot P, Flechon JE (1970b) Forme et voie d'absorption intestinale des acides gras à chaîne longue chez la truite arc-en-ciel Salmo gairdneri R. II. Lipides étalés. Ann Biol Anim Biochim Biophys 10:473–480

    Google Scholar 

  • Burnstock G (1959) The morphology of the gut of the brown trout (Salmo trutta). Q J Microsc Sci 100:183–198

    Google Scholar 

  • Castell JD, Sinnhuber RO, Wales JH, Lee DJ (1972) Essential fatty acids in the diet of rainbow trout (Salmo gairdneri). Growth, feed conversion and some gross dificiency symptoms. J Nutr 102:77–85

    Google Scholar 

  • Colin DA, Nonnotte G, Leray C, Nonnotte L (1985) Na transport and enzyme activities in the intestine of the freshwater and seawater adapted trout (Salmo gairdneri R.) Comp Biochem Physiol 81A, 3:695–698

    Google Scholar 

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

    Google Scholar 

  • Ezeasor DN, Stokoe WM (1980) Scanning electron microscopic study of the gut mucosa of the rainbow trout Salmo gairdneri R. J Fish Biol 17:529–539

    Google Scholar 

  • Ezeasor DN, Stokoe WM (1981) Light and electron microscopic studies on the absorptive cells of the intestine, caeca and rectum of the adult rainbow trout Salmo gairdneri R. J Fish Biol 18:527–544

    Google Scholar 

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

    Google Scholar 

  • Field M, Karnaky KJ, Smith P, Bolton JE, Kinter WB (1978) Ion transport across the isolated intestinal mucosa of the winter Flounder, Pseudopleuronectes americanus. J Membr Biol 41:265–293

    Google Scholar 

  • Gas-Baby N (1976) Cytophysiologie de l'appareil digestif et du tissu musculaire de la carpe. Modifications structurales et fonctionnelles induites par le jeûne et la réalimentation. Thèse d'Etat, Biologie cellulaire, Toulouse

  • Goodman DBP, Davis WL, Jones RG (1980) Glyoxylate cycle in toad urinary bladder: possible stimulation by aldosterone. Proc Natl Acad Sci USA 77, 3:1521–1525

    Google Scholar 

  • Gordon MS (1959) Ionic regulation in the brown trout (Salmotrutta L.). J Exp Biol 36:227–252

    Google Scholar 

  • Greene CW (1912) Anatomy and histology of the alimentary tract of the king salmon. Bur Fish Bull 32:73–100

    Google Scholar 

  • Gulland GL (1898) The minute structure of the digestive tract of the king salmon and the changes which occur in freshwater. Anat Anz 14:441–445

    Google Scholar 

  • Hirano T, Mayer-Gostan N (1976) Eel oesophagus as an osmoregulatory organ. Proc Natl Acad Sci USA 73:1348–1350

    Google Scholar 

  • Hirano T, Morisawa M, Ando M, Utida S (1976) Adaptative changes in ion and water transport mechanism in the eel intestine ion transport. In: Robinson JW (ed) Intestinal ion transport. MTP Press Ltd, Lancaster, 301, 317

    Google Scholar 

  • Iwai T (1968) Fine structure and absorption patterns of intestinal epithelial cells in rainbow trout alevins. Z Zellforsch 91:368–379

    Google Scholar 

  • Kaye GI, Wheeler HO, Whitlock RT, Lane N (1966) Fluid transport in the rabbit gallbladder. A combined physiological and electron microscopy study. J Cell Biol 30:237–268

    Google Scholar 

  • Lahlou B (1976) Ionic permeability of fish intestinal mucosa in relation to hypophysectomy and salt adaptation. In: Robinson JWL (ed) Intestinal ion transport. MTP Press, Lancaster, pp 318–328

    Google Scholar 

  • Laurent P, Kirsch R (1975) Modifications structurales de l'oesophage liées à l'osmorégulation chez l'Anguille. CR Acad Sci 280:2227–2229

    Google Scholar 

  • Leray C, Florentz A (1983) Biochemical adaptation of trout intestine related to its ion transport properties. Influences of dietary salt and fatty acids, and environmental salinity. In: Gilles-Baillien M, Gilles R (eds) Intestinal transport. Springer, Berlin Heidelberg New York Tokyo, pp 354–368

    Google Scholar 

  • Leray C, Colin DA, Florentz A (1981) Time course of osmotic adaptation and gill energetics of Rainbow trout (Salmo gairdneri R.) following abrupt changes in external salinity. J Comp Physiol 144:175–181

    Google Scholar 

  • Loeschke K, Bentzel CJ, Csaky T (1970) Asymmetry of osmotic flow in frog intestine: functional and structural correlation. Am J Physiol 218, 6:1723–1731

    Google Scholar 

  • Nonnotte G, Colin DA, Aubrée A, Nonnotte L, Leray C (1984) Transports ioniques et métabolisme énergétique intestinaux chez la truite au cours de l'adaptation à l'eau de mer. J Physiol (Paris) 79, 5:82A

  • Ozaki N (1965) Some observations on the fine structure of the intestinal epithelium in some marine teleosts. Arch Histol Jpn 26:23–38

    Google Scholar 

  • Peaker M, Linsell JC (1975) Salt glands in birds and reptiles. Cambridge University Press, Cambridge

    Google Scholar 

  • Porthe-Nibelle J, Lahlou B (1974) Plasma concentration of cortisol in hypophysectomized and sodium chloride-adapted goldfish (Carassius auratus L.). J Endocrinol 63:377–387

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Rhodin J (1958) Anatomy of kidney tubules. Int Rev Cyto 7:485–499

    Google Scholar 

  • Robinson JS, Mead JF (1973) Lipid absorption and deposition in rainbow trout (Salmo gairdneri). Can J Biochem 51:1050–1058

    Google Scholar 

  • Rostgaard J, Frederiksen O (1981) Fluid transport and dimensions of epithelial cells and intercellular spaces in frog gallbladder. Cell Tissue Res 215:223–247

    Google Scholar 

  • Sharratt BM, Bellamy D, Jones IC (1964) Adaptation of the silver eel (Anguilla anguilla L.) to sea water and to artificial media together with observations on the role of the gut. Comp Biochem Physiol 11:19–30

    Google Scholar 

  • Shehadeh ZH, Gordon MC (1969) The role of the intestine in salinity adaptation of the rainbow trout Salmo gairdneri. Comp Biochem Physiol 30:397–418

    Google Scholar 

  • Sire MF, Vernier JM (1981) Etude ultrastructurale de la synthèse de chylomicron au cours de l'absorption intestinale des lipides chez la truite. Influence de la nature des acides gras ingérés. Biol Cell 40:47–62

    Google Scholar 

  • Sire MF, Lutton C, Vernier JM (1981) New views on intestinal absorption of lipids in teleostean fishes: An ultrastructural and biochemical study in the rainbow trout. J Lipid Res 22:81–94

    Google Scholar 

  • Skadhauge E (1969) The mechanism of salt and water absorption in the intestine of the eel (Anguilla anguilla) adapted to waters of various salinities. J Physiol 204:135–158

    Google Scholar 

  • Spring KR, Hope A (1978) Size and shape of the lateral intercellular spaces in a living epithelium. Science 200:54–58

    Google Scholar 

  • Spring KR, Hope A (1979) Fluid transport and the dimension of cells and interspaces of living Necturus gall-bladder. J Gen Physiol 73:287–305

    Google Scholar 

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

    Google Scholar 

  • Wedemeyer G (1972) Some physiological consequences of handling stress in the juvenile Coho salmon (Oncorhynchus kisutch) and steelhead trout (Salmo gairdneri). J Fish Res Bd Canada 29:1780–1783

    Google Scholar 

  • Weinreb EL, Bilstad NM (1955) Histology of the digestive tract and adjacent structures of the rainbow trout, Salmo gairdneri widens. Copeia 3:194–204

    Google Scholar 

  • Yamamoto T (1966) An electron microscopic study on the columnar epithelial cell of freshwater teleosts: goldfish (Carassius auratus) and rainbow trout (Salmo irideus). Z Zellforsch 72:66–87

    Google Scholar 

  • Yamamoto M, Hirano T (1978) Morphological changes in the oesophageal epithelium of the eel Anguilla japonica during adaptation to seawater. Cell Tissue Res 192:25–38

    Google Scholar 

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  1. C.N.R.S., Strasbourg, France

    Liliane Nonnotte, Guy Nonnotte & Claude Leray

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  1. Liliane Nonnotte
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  2. Guy Nonnotte
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  3. Claude Leray
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Nonnotte, L., Nonnotte, G. & Leray, C. Morphological changes in the middle intestine of the rainbow trout, Salmo gairdneri, induced by a hyperosmotic environment. Cell Tissue Res. 243, 619–628 (1986). https://doi.org/10.1007/BF00218070

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