NaCl Transport in Salt Glands

  • E. Schlatter
  • R. Greger
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 1)


Thirty years ago Schmidt-Nielsen and his co-workers described a salt-secreting supraorbital nasal gland in marine birds (K. Schmidt-Nielsen et al. 1957, 1958). The avian salt gland was the second extrarenal organ after the gills of fish that was found to participate in the osmoregulation in marine animals. Later, other homologous and nonhomologous exocrine salt glands have been described in a variety of vertebrates such as the lacrimal gland of turtles (K. Schmidt-Nielsen and Fänge 1958), the sublingual gland of sea snakes (K. Schmidt-Nielsen and Fänge 1958), the rectal gland of elasmobranchs (Burger and Hess 1960), the nasal salt gland in some terrestrial birds (K. Schmidt-Nielsen et al. 1963), the nasal salt glands of various reptiles (W. A. Dunson 1976; K. Schmidt-Nielsen et al. 1963; Templeton 1964), and the dendritic organ of marine catfish (van Lennep and Lanzing 1967). The term “salt gland” is generally used for extrarenal salt-excreting glands in vertebrates (van Lennep and Young 1979). However, glandular organs with a similar osmoregulatory function have also been described in invertebrates, such as the crustacean salt glands (Conte 1984; Copeland 1967).


Basolateral Membrane Salt Gland Salt Loading Rectal Gland Spiny Dogfish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrews SB, Mazurkiewicz JE, Kirk GR (1983) The distribution of intracellular ions in the avian salt gland. J Cell Biol 96:1389–1399PubMedGoogle Scholar
  2. Barrnett RJ, Mazurkiewicz JE, Addis JS (1983) Avian salt gland: a model for the study of membrane biogenesis. In: Fleischer S, Fleischer B (eds), vol 96. Academic Press, London New York, pp 627–659Google Scholar
  3. Bradshaw SD, Lemire M, Vernet R, Grenot CJ (1984 a) Aldosterone and the control of secretion by the nasal salt gland of the North African desert lizard, Uromastix acanthinurus. Gen Comp Endocrinol 54:314–323PubMedGoogle Scholar
  4. Bradshaw SD, Tom JA, Bunn SE (1984b) Corticosteroids and control of nasal salt gland function in the lizard Tiliqua rugosa. Gen Comp Endocrinol 54:308–313PubMedGoogle Scholar
  5. Burger JW, Hess WN (1960) Function of the rectal gland in the spiny dogfish. Science 131:670 – 671PubMedGoogle Scholar
  6. Butler DG (1980) Functional nasal glands in adrenalectomized domestic ducks (Anas platyrhynchos). Gen Comp Endocrinol 40:15–26PubMedGoogle Scholar
  7. Butler DG (1984) Endocrine control of the nasal salt glands in birds. J Exp Zool 232:725 – 736PubMedGoogle Scholar
  8. Conte FP (1984) Structure and function of the crustacean larval salt gland. Int Rev Cytol 91:45 – 104Google Scholar
  9. Copeland DE (1967) A study of salt secreting cells in the brine shrimp Artemia salina. Protoplasma 63:363–384PubMedGoogle Scholar
  10. Cowan FBM (1974) Observations on extrarenal excretion by orbital glands and osmoregulation in Malaclemys terrapin. Comp Biochem Physiol A 48:489–500PubMedGoogle Scholar
  11. Degnan KJ, Karnaky KJ, Zadunaisky JA (1977) Active chloride transport in the in vitro opercular skin of teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells. J Physiol (London) 271:155–191Google Scholar
  12. Deutsch H, Hammel HT, Simon E, Simon-Oppermann C (1979) Osmolality and volume factors in salt gand control of Pekin ducks after adaptation to chronic salt loading. J Comp Physiol 129:301–308Google Scholar
  13. Dunson MK, Dunson WA (1974) The relation between plasma Na concentration and salt gland Na-K ATPase content in the diamond backed terrapin and the yellow-bellied sea snake. J Comp Physiol 101:89–97Google Scholar
  14. Dunson WA (1969) Electrolyte excretion by the salt gland. Am J Physiol 216:995 – 1002PubMedGoogle Scholar
  15. Dunson WA (1976) Salt glands in reptiles. In: Gans C, Dunson WR (eds) Biology of the Reptilia, vol 5. Physiology A, Academic Press, London New York, pp 413–445Google Scholar
  16. Dunson WA (1979) Control mechanisms in reptiles. In: Gilles R (ed) Mechanisms of osmoregulation in animals: maintenance of cell volume. Wiley, New York, pp 273 – 322Google Scholar
  17. Dunson WA, Dunson MK (1973) Convergent evolution of sublingual salt glands in the marine file snake and the true sea snakes. J Comp Physiol 86:193–208Google Scholar
  18. Dunson WA, Dunson MK, Ohmart RD (1976) Evidence for the presence of nasal salt glands in the roadrunner and the Cortunix quail. J Exp Zool 198:209–216PubMedGoogle Scholar
  19. Ellis RA, Goertemiller CC Jr (1974) Cytological effects of salt-stress and localization of transport adenosine triphosphatase in the lateral nasal salt glands of the desert iguana, Dipsosaurus dorsalis. Anat Rec 180:285–297PubMedGoogle Scholar
  20. Emery N, Poulson TL, Kinter WB (1972) Production of concentrated urine by avian kidneys. Am J Physiol 223:180–187PubMedGoogle Scholar
  21. Epstein FH (1979) The shark rectal gland: a model for the active transport of chloride. Yale J Biol Med 52:517–523PubMedGoogle Scholar
  22. Ernst SA, Ellis RA (1969) The development of surface specilization in the secretory epithelium of the avian salt gland in response to osmotic stress. J Cell Biol 40:305 – 321PubMedGoogle Scholar
  23. Ernst SA, Mills JW (1977) Basolateral plasma membrane localization of ouabain-sensitive sodium transport sites in the secretory epithelium of the avian salt gland. J Cell Biol 75:74–94PubMedGoogle Scholar
  24. Ernst SA, Rossum GDV van (1982) Ions and energy metabolism in duck salt-gland: possible role of furosemide-sensitive co-transport of sodium and chloride. J Physiol (London) 325:333–352Google Scholar
  25. Ernst SA, Riddle CV, Karnaky KJ (1980) Relationship between localization of the (Na++K+)- ATPase, cellular fine structure, and reabsorptive and secretory electrolyte transport. In: Boulpaep EL (Ed) Current topics in membranes and transport, vol 13. Academic Press, London New York, pp 335–385Google Scholar
  26. Fänge RK, Schmidt-Nielsen K, Robinson M (1958) Control of secretion from the avian salt gland. Am J Physiol 195 (2):321 – 326PubMedGoogle Scholar
  27. Fisher SK, Hootman SR, Hancock AM, Ernst SA, Agranoff BW (1983) Muscarinic stimulation of phospholipid turnover in dissociated salt gland cells. FEBS Lett 155:43–46PubMedGoogle Scholar
  28. Flechter GL, Stainer IM, Holmes WN (1967) Sequential changes in adenosine triphosphatase activity and the electrolyte capacity of the nasal-glands of the duck during the period of adaptation to saltwater. J Exp Biol 47:375–391Google Scholar
  29. Frizzell RA, Field M, Schultz SG (1979) Sodium-coupled chloride transport by epithelial tissues. Am J Physiol 236:F1–F8PubMedGoogle Scholar
  30. Geck P, Heinz E (1986) The Na-K-2Cl cotransport system. J Membr Biol 91:97–105PubMedGoogle Scholar
  31. Geck P, Pietryzk C, Burckhardt BC, Pfeiffer B, Heinz E (1980) Electrically silent cotransport of Na+, K+ and Cl- in Ehrlich cells. Biochim Biophys Acta 600:432–447PubMedGoogle Scholar
  32. Gilmore JP, Dietz J, Gilmore C, Zucker IH (1977) Evidence for a chloride pump in the salt gland of the goose. Comp Biochem Physiol 56A:121 – 126Google Scholar
  33. Gögelein H, Schlatter E, Greger R (1987 a) The “small” conductance chloride channel in the luminal membran of the rectal gland of the dogfish (Squalus acanthias). Pfluegers Arch 409: 122–125Google Scholar
  34. Gögelein H, Greger R, Schlatter E (1987 b) Potassium channels in the basolateral membrane of the rectal gland of Squalus acanthias. Regulation and inhibitors. Pfluegers Arch 409:107–113Google Scholar
  35. Greger R (1985) Ion transport mechanisms in thick ascending limb of Henle’s loop of mammalian nephron. Physiol Rev 65:760–797PubMedGoogle Scholar
  36. Greger R, Schlatter E (1981) Presence of luminal K+, a prerequisite for active NaCl transport in the cortical thick ascending limb of Henle’s loop of rabbit kidney. Pfluegers Arch 392:92–94Google Scholar
  37. Greger R, Schlatter E (1983 a) Properties of the basolateral membrane of the cortical thick ascending limb of Henle’s loop of rabbit kidney. A model for secondary active chloride transport. Pfluegers Arch 396:325–334Google Scholar
  38. Greger R, Schlatter E (1983 b) Cellular mechanism of the action of loop diuretics on the thick ascending limb of Henle’s loop. Klin Wochenschr 61:1019–1027PubMedGoogle Scholar
  39. Greger R, Schlatter E (1984 a) Mechanism of NaCl secretion in the rectal gland of spiny dogfish (Squalus acanthias). I. Experiments in isolated in vitro perfused rectal gland tubules. Pfluegers Arch 402:63–75Google Scholar
  40. Greger R, Schlatter E (1984 b) Mechanism of NaCl secretion in the rectal gland of spiny dogfish (Squalus acanthias). II. Effects of inhibitors. Pfluegers Arch 402:364–375Google Scholar
  41. Greger R, Schlatter E, Lang F (1983) Evidence for electroneutral sodium chloride cotransport in the cortical thick ascending limb of Henle’s loop of rabbit kidney. Pfluegers Arch 396:308–314Google Scholar
  42. Greger R, Schlatter E, Wang F, Forrest JN Jr (1984) Mechanism of NaCl secretion in rectal gland tubules of spiny dogfish (Squalus acanthias). III. Effects of stimulation of secretion by cAMP. Pfluegers Arch 402:376 – 384Google Scholar
  43. Greger R, Schlatter E, Gögelein H (1985) Cl- channels in the apical cell membrane of the rectal gland “induced” by cAMP. Pfluegers Arch 403:446–448Google Scholar
  44. Greger R, Schlatter E, Gögelein H (1986) Sodium chloride secretion in rectal gland of dogfish (Squalus acanthias). New trends in physiology. Science 1:134 – 136Google Scholar
  45. Greger R, Gögelein H, Schlatter E (1987 a) Potassium channels in the basolateral membrane of the rectal gland of the dogfish (Squalus acanthias). Pfluegers Arch 409:100–106Google Scholar
  46. Greger R, Schlatter E, Gögelein H (1987 b) Chloride channels in the luminal membrane of the rectal gland of the dogfish (Squalus acanthias). Properties of the “larger” conductance channel. Pfluegers Arch 409:114–121Google Scholar
  47. Hannafin J, Kinne-Saffran E, Frieman D, Kinne R (1983) Presence of a sodium-potassium chloridecotransport system in the rectal gland of Squalus acanthias. J Membr Biol 75:73 – 83PubMedGoogle Scholar
  48. Harvey S, Phillips JG (1982) Endocrinology of salt gland function. Comp Biochem Physiol 71A: 537–546Google Scholar
  49. Harvey S, Phillips JG, Rees A (1984) Independence of salt gland function and adrenocortical activityin ducks (Anas platyrhynchos). Gen Comp Endocrinol 60:210–214Google Scholar
  50. Hayslett JP, Gögelein H, Greger R (1987) Characteristics of apical chloride channels in human colon cells (HT29). Pfluegers Arch (in press)Google Scholar
  51. Holmes WN (1972) Regulation of electrolyte balance in marine birds with special reference to the role of the pituitary-adrenal axis in the duck (Anasplatyrhynchos). Fed Proc 31:1587–1598PubMedGoogle Scholar
  52. Holmes WN (1975) Hormones and osmoregulation in marine birds. Gen Comp Endocrinol 25:249–258PubMedGoogle Scholar
  53. Holmes WN, Phillips JG (1985) The avian salt gland. Biol Rev 60:213–256Google Scholar
  54. Holmes WN, Stewart DJ (1968) Changes in the nucleic acid and protein composition of the nasal glands from the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. J Exp Biol 48:509–519PubMedGoogle Scholar
  55. Hootman SR, Ernst SA (1981) Effect of methacholine on Na+ pump activity and ion content of dispersed avian salt gland cells. Am J Physiol 241:R77–R86PubMedGoogle Scholar
  56. Kirschner LB (1977) The sodium chloride excreting cells in marine vertebrates. In: Gupta BL, Moreton RB, Oshman JL, Wall BW (eds) Transport of ions and water in animals. Academic Press, London New York, pp 427–452Google Scholar
  57. Kirschner LB (1980) Comparison of vertebrate salt excreting organs. Am J Physiol 238:R219–R223PubMedGoogle Scholar
  58. Lennep EW van, Lanzing WJR (1967) The ultrastructure of glandular cells in the external dendritic organ of some marine catfish. J Ultrastruct Res 18:333–344PubMedGoogle Scholar
  59. Lennep EW van, Young JA (1979) Salt glands. In: Giebisch G (ed) Transport organs. Membrane transport in biology, vol 4B. Springer, Berlin Heidelberg New York, pp 675 – 692Google Scholar
  60. Lingham RB, Stewart DJ, Sen AK (1980) The induction of (Na+ +K+)-ATPase in salt gland of the duck. Biochim Biophys Acta 601:229 – 234PubMedGoogle Scholar
  61. Lowy RJ, Dawson DC, Ernst SA (1985) Primary culture of duck salt gland. II Neurohormonal stimulation of active transport. Am J Physiol 249: C41 –C47PubMedGoogle Scholar
  62. Marshall AT, Hyatt AD, Phillips JG, Condron RJ (1985) Isosmotic secretion in the avian nasal salt gland: X-ray microanalysis of luminal and intracellular ion distributions. J Comp Physiol B 156:213–227Google Scholar
  63. Merchant JL, Papermaster DS, Barnett RJ (1985) Correlation of (Na+ + K+)-ATPase content and plasma membrane surface area in adapted and de-adapted salt glands of ducklings. J Cell Sci 78:233–246PubMedGoogle Scholar
  64. Osmolska H (1979) Nasal salt gland in dinosaurs. Acta Palaeontol Pol 24:205–215Google Scholar
  65. Palfrey HC, Silva P, Epstein FH (1984) Sensitivity of cAMP-stimulated salt secretion in shark rectal gland to “loop” diuretics. Am J Physiol 246:C242–C246PubMedGoogle Scholar
  66. Peaker M (1979) Control mechanisms in birds. In: Gilles R (ed) Mechanisms of osmoregulation in animals. Wiley, New York, pp 323 – 348Google Scholar
  67. Peaker M, Linzell JL (1975) Salt glands in birds and reptiles. Cambridge Univ Press, LondonGoogle Scholar
  68. Peaker M, Stockley SJ (1974) The effects of lithium and methacholine on the intracellular ionic composition of goose salt gland slices: relation to sodium and chloride transport. Experientia 30:158–159PubMedGoogle Scholar
  69. Petersen OH, Maruyama Y (1984) Calcium-activated potassium channels and their role in secretion. Nature (London) 307:693 – 696Google Scholar
  70. Reuss L, Reinach P, Weinman SA, Grady TP (1983) Intracellular ion activities and Cl- transport mechanisms in bullfrog corneal epithelium. Am J Physiol 244:C336–C347PubMedGoogle Scholar
  71. Riddle CV, Ernst SA (1979) Structural simplicity of the zonula occludens in the electrolyte secreting epithelium of the avian salt gland. J Membr Biol 45:21–35PubMedGoogle Scholar
  72. Rossum GDV van (1966) Movements of Na+ and K+ in slices of herring gull salt gland. Biochim Biophys Acta 126:338 – 349PubMedGoogle Scholar
  73. Saint-Girons H, Lemke M, Bradshaw SD (1977) Structure de la glande nasale externe de Tiliqua rugosa (Reptilia, scincidae) et rapports avec sa fonction. Zoomorphologie 88:277–288Google Scholar
  74. Schlatter E, Greger R, Weidtke C (1983) Effect of “high ceiling” diuretics on active salt transport in the cortical thick ascending limb of Henle’s loop of rabbit kidney. Correlation of chemical structure and inhibitory potency. Pfluegers Arch 396:210–217Google Scholar
  75. Schmidt-Nielsen B (1976) Intracellular concentrations of the salt gland of the herring gull Larus argentatus. Am J Physiol 230:514–521PubMedGoogle Scholar
  76. Schmidt-Nielsen K (1960) The salt secreting gland of marine birds. Circulation 21:955–967PubMedGoogle Scholar
  77. Schmidt-Nielsen K, Fänge R (1958) Salt glands in marine reptiles. Nature (London) 182:783–785Google Scholar
  78. Schmidt-Nielsen K, Jörgensen CB, Osaki H (1957) Secretion of hypertonic solutions in marine birds. Fed Proc 16:113–114Google Scholar
  79. Schmidt-Nielsen K, Jörgensen CB, Osaki H (1958) Extrarenal salt excretion in birds. Am J Physiol 193:101–107PubMedGoogle Scholar
  80. Schmidt-Nielsen K, Borut A, Lee P, Crawford E (1963) Nasal salt secretion and the possible function of the cloaca in water conservation. Science 142:1300–1301Google Scholar
  81. Serventy DL (1971) Biology of desert birds. In: Farner DS, King JR (eds) Avian biology, vol 1, Academic Press, London New York, pp 287 – 339Google Scholar
  82. Shoemaker VH, Nagy KA, Bradshaw SD (1972) Studies on the control of electrolyte excretion by the nasal gland of the lizard Dipsosaurus dorsalis. Comp Biochem Physiol A 42:749 – 757PubMedGoogle Scholar
  83. Shorofsky SR, Field M, Fozzard HA (1982) The cellular mechanism of active chloride secretion in vertebrate epithelia: studies in intestine and trachea. Philos Trans R Soc London Ser B 299:597–607Google Scholar
  84. Shuttleworth TJ, Thorndyke MC (1984) An endogenous peptide stimulates secretory activity in the elasmobranch rectal gland. Science 225:319–321PubMedGoogle Scholar
  85. Silva P, Stoff J, Field M, Fine L, Forrest JN, Epstein FH (1977) Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport. Am J Physiol 233: F298–F306PubMedGoogle Scholar
  86. Silva P, Stoff JS, Solomon RJ, Rosa R, Stevens A, Epstein J (1980) Oxygen cost of chloride transport in perfused rectal gland of Squalus acanthias. J Membr Biol 53:215–221Google Scholar
  87. Silva P, Stoff JS, Leone DR, Epstein FH (1985) Mode of action of somatostatin to inhibit secretion by shark rectal gland. Am J Physiol 249:R329–R334PubMedGoogle Scholar
  88. Silva P, Stoff JS, Solomon RJ (1987) Atrial natriuretic peptide stimulates salt secretion by shark rectal gland by releasing VIP. Am J Physiol 252:F99–F103PubMedGoogle Scholar
  89. Simon E (1982) The osmoregulatory system of birds with salt glands. Comp Biochem Physiol 71A:547–556Google Scholar
  90. Skou JC (1975) The (Na+ + K+)-activated enzyme system and its relationship to transport of sodium and potassium. Q Rev Biophys 7:401 – 434Google Scholar
  91. Snider RM, Roland RM, Lowy RJ, Agranoff BW, Ernst SA (1968) Muscarinic receptor-stimulated Ca2+ signaling and inositol lipid metabolism in avian salt gland cells. Biochim Biophys Acta 889:216–224Google Scholar
  92. Solomon R, Taylor M, Stoff JS, Silva P, Epstein FH (1984) In vivo effect of volume expansion on rectal gland function. I. Humoral factors. Am J Physiol 246:R63–R66PubMedGoogle Scholar
  93. Solomon R, Taylor M, Sheth S, Silva P, Epstein EH (1985 a) Primary role of volume expansion in stimulation of rectal gland function. Am J Physiol 248:R638–R640PubMedGoogle Scholar
  94. Solomon R, Taylor M, Dorsey D, Silva P, Epstein FH (1985 b) Atriopeptin stimulation of rectal gland function in Squalus acanthias. Am J Physiol 249:R348 – R354PubMedGoogle Scholar
  95. Stewart DJ, Semple EW, Swart GT, Sen AK (1976) Induction of the catalytic protein of (Na+ + K+)-ATPase in the salt gland of the duck. Biochim Biophys Acta 419:150–163PubMedGoogle Scholar
  96. Stewart DJ, Sax J, Funk R, Sen AK (1979) Possible role of cyclic GMP in stimulus-secretion coupling by salt gland of the duck. Am J Physiol 237:C200–C204PubMedGoogle Scholar
  97. Taplin LE, Griff GC (1981) Salt glands in the tongue of the estuarine crocodile Crocodylus porosus. Science 212:1045–1047PubMedGoogle Scholar
  98. Templeton JR (1964) Nasal salt excretion in terrestrial lizards. Comp Biochem Physiol 11:223–229PubMedGoogle Scholar
  99. Thesleff S, Schmidt-Nielsen K (1962) An electrophysiological study of the salt gland of the herring-gull. Am J Physiol 202:597–600PubMedGoogle Scholar
  100. Thomas DH, Phillips JG (1975) Studies in avian adrenal steroid function. IV Adrenalectomy and the response of the domestic duck (Anas platyrhynchos) to hypertonic NaCl loading. Gen Comp Endocrinol 26:412–419Google Scholar
  101. Wangemann P, Wittner M, Di Stefano A, Englert HC, Lang HJ, Schlatter E, Greger R (1986) Cl--channel blockers in the thick ascending limb of the loop of Henle. Structure activity relationship. Pfluegers Arch 407 (Suppl 2):S128 – 141Google Scholar
  102. Welsh MJ (1983) Intracellular chloride activities in canine tracheal epithelium. Direct evidence for sodium-coupled intracellular chloride accumulation in a chloride-secreting epithelium. J Clin Invest 71:1392–1401PubMedGoogle Scholar
  103. Welsh MJ, Smith PL, Fromm M, Frizzell RA (1982) Crypts are the site of intestinal fluid and electrolyte secretion. Science 218:1219–1221PubMedGoogle Scholar
  104. Wilson JX (1984) The renin-angiotensin system and the nervous control of blood circulation. Endocrinol Rev 5:45–61Google Scholar
  105. Wilson JX, Pham D van, Tau-Wilson HI (1985) Angiotensin and converting enzyme regulate extrarenal salt excretion in ducks. Endocrinology 117:135–140PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1988

Authors and Affiliations

  • E. Schlatter
    • 1
  • R. Greger
    • 1
  1. 1.Physiologisches Institut der Albert-Ludwigs-UniversitätFreiburgGermany

Personalised recommendations