Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys: Implications for osmoregulation in fresh and seawater

Journal of Experimental Biology

Volumn 207, Issue 20, 2004, Pages 3447-3462

  Bartels, Helmut ^a   Potter, Ian C ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b MURDOCH UNIVERSITY   (Australia)

Author keywords

Agnatha; Chloride cell; Gill epithelium; Lamprey; Mitochondria rich cell; Osmoregulation; Pavement cell

Indexed keywords

CHLORIDE; FRESH WATER; SEA WATER; SODIUM;

ANIMAL; CYTOLOGY; ELECTROLYTE BALANCE; EPITHELIUM; GILL; HISTOLOGY; LAMPREY; LARVA; METABOLISM; MITOCHONDRION; PHYSIOLOGY; REVIEW; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; CHLORIDES; EPITHELIUM; FRESH WATER; GILLS; LAMPREYS; LARVA; MICROSCOPY, ELECTRON, SCANNING; MITOCHONDRIA; SEAWATER; SODIUM; WATER-ELECTROLYTE BALANCE;

AGNATHA; PETROMYZONTIDAE; PISCES; TELEOSTEI; VERTEBRATA;

EID: 6344233643     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01157     Document Type: Review

References (127)

1. +-ATPase. Proc. Natl. Acad. Sci. USA 86, 5429-5433.
2. Bartels, H. (1989). Freeze-fracture study of the pavement cell in the lamprey gill epithelium. Analogy of membrane structure with the granular cell in the amphibian urinary bladder. Biol. Cell 66, 165-171.
3. Bartels, H. and Potter, I. C. (1991). Structural changes in the zonulae occludentes of the chloride cells of young adult lampreys following acclimation to seawater. Cell Tissue Res. 265, 447-457.
4. Bartels, H. and Potter, I. C. (1993). Intercellular junctions in the water-blood barrier of the gill lamella in the adult lamprey (Geotria australis, Lampetra fluviatilis). Cell Tissue Res. 274, 521-532.
5. Bartels, H. and Welsch, U. (1986). Mitochondria-rich cells in the gill epithelium of cyclostomes. A thin section and freeze fracture study. In Proceedings of the Second International Conference on Indo-Pacific Fishes (ed. T. Uyeno, R. Arai, T. Taniuchi and K. Matsuura), pp. 58-72. Tokyo: Ichthyological Society of Japan.
6. Bartels, H., Schewe, H. and Potter, I. C. (1993). Structural changes in the apical membrane of lamprey chloride cells after acclimation to seawater. Am. J. Physiol. 265, C733-C739.
7. Bartels, H., Moldenhauer, A. and Potter, I. C. (1996). Changes in the apical surface of chloride cells following acclimation of lampreys to seawater. Am. J. Physiol. 270, R125-R133.
8. Bartels, H., Potter, I. C., Pirlich, K. and Mallatt, J. (1998). Categorization of the mitochondria-rich cells in the gill epithelium of the freshwater phases in the life cycle of lampreys. Cell Tissue Res. 291, 337-349.
9. Beamish, F. W. H. (1980). Osmoregulation in juvenile and adult lampreys. Can. J. Fish. Aquat. Sci. 37, 1739-1750.
10. Beamish, F. W. H., Strachan, P. D. and Thomas, E. (1978). Osmotic and ionic performance of the anadromous sea lamprey, Petromyzon marinus. Comp. Biochem. Physiol. A 60, 435-443.
11. Bentley, P. J. (1962). Permeability of the skin of the cyclostome Lampetra fluviatilis to water and electrolytes. Comp. Biochem. Physiol. 6, 95-97.
12. Bentley, P. J. and Follett, B. K. (1962). The action of neurohypophysial and adrenocortical hormones on sodium balance in the cyclostome, Lampetra fluviatis. Gen. Comp. Endocrinol. 2, 329-335.
13. Bentley, P. J. and Follett, B. K. (1963). Kidney function in a primitive vertebrate, the cyclostome Lampetra fluviatilis. J. Physiol. (Lond.) 169, 902-918.
14. Biemesderfer, D., Stanton, B., Wade, J. B., Kashgarian, M. and Giebisch, G. (1989). Ultrastructure of Amphiuma distal nephron: evidence for cellular heterogeneity. Am. J. Physiol. 256, C849-C857.
15. Bourguet, J., Chevalier, J. and Hugon, J. S. (1976). Alterations in membrane-associated particle distribution during antidiuretic challenge in frog urinary bladder. Biophys. J. 16, 627-639.
16. Brown, D. (1989). Membrane recycling and epithelial cell function. Am. J. Physiol. 256, F1-F12.
17. Brown, D. and Breton, S. (1996). Mitochondria-rich, proton-secreting epithelial cells. J. Exp. Biol. 199, 2345-2358.
18. +V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J. Exp. Biol. 203, 137-145.
19. +-ATPase. J. Cell Biol. 105, 1637-1648.
20. +-ATPase is present in opposite plasma membrane domains in subpopulations of kidney epithelial cells. Nature 331, 622-624.
21. Brown, D., Katsura, T., Kawashima, M., Verkman, A. S. and Sabolic, I. (1995). Cellular distribution of the aquaporins: a family of water channel proteins. Histochem. Cell Biol. 104, 1-9.
22. Cerejido, M., Gonzalez-Mariscal, L. and Contreras, G. (1989). Tight junction: barrier between higher organisms and environment. NIPS 4, 72-75.
23. Cholette, C., Gagnon, A. and Germain, P. (1970). Isosmotic adaption in Myxine glutinosa L. I. Variations of some parameters and role of the amino acid pool of the muscle cells. Comp. Biochem. Physiol. 33, 333-346.
24. Claude, P. (1978). Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludens. J. Membr. Biol. 39, 219-232.
25. Claude, P. and Goodenough, D. A. (1973). Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J. Cell Biol. 58, 390-400.
26. +-ATPase and carbonic anhydrase activity in gills of 17 fish species. Can. J. Zool. 66, 2398-2405.
27. Delarbre, C., Gallut, C., Barriel, V., Janvier, P. and Gachelin, G. (2002). Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: The comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly. Mol. Phylog. Evol. 22, 184-192.
28. DiBona, D. R., Civan, M. M. and Leaf, A. (1969). The cellular specificity of the effect of vasopressin on toad urinary bladder. J. Membr. Biol. 1, 79-91.
29. Durham, J. H. and Nagel, W. (1986). Evidence for separate cellular origins of sodium and acid-base transport in the turtle bladder. Am. J. Physiol. 250, C609-C616.
30. + transport processes in frog skin. J. Exp. Biol. 200, 247-256.
31. Ehrenfeld, J., Lacoste, I. and Harvey, B. J. (1989). The key role of mitochondria-rich cells in Na and H transport across the frog skin epithelium. Pflügers Arch. 414, 59-67.
32. Eriksson, Ö., Mayer-Gostan, N. and Wistrand, P. J. (1985). The use of isolated fish opercular epithelium as a model tissue for studying intrinsic activities of loop diuretics. Acta Physiol. Scand. 125, 55-66.
33. Ernst, S. A., Dodson, W. B. and Karnaky, K. J., Jr (1980). Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heieroclitus). J. Cell Biol. 87, 488-497.
34. Ernst, S. A., Hootman, S. R., Schreiber, J. H. and Riddle, C. V. (1981). Freeze-fracture and morphometric analysis of occluding junctions in rectal glands of elasmobranch fish. J. Membr. Biol. 58, 101-114.
35. Forey, P. L. and Janvier, P. (1993). Agnathans and the origin of jawed vertebrates. Nature 361, 129-134.
36. Foskett, J. K. and Machen, T. E. (1985). Vibrating probe analysis of teleost opercular epithelium: correlation between active transport and leak pathways of individual chloride cells. J. Membr. Biol. 85, 25-35.
37. Foskett, J. K. and Scheffey, C. (1982). The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215, 164-166.
38. -independent transport across the skin of Rana esculenta. Am. J. Physiol. 228, 839-844.
39. Garty, H. (1986). Mechanisma of aldosterone action in tight epithelia. J. Membr. Res. 90, 193-205.
40. Garty, H. and Palmer, L. G. (1997). Epithelial sodium channels: function, structure and regulation. Physiol. Rev. 77, 359-396.
41. Goss, G. G., Laurent, P. and Perry, S. F. (1992). Evidence for a morphological component in the regulation of acid-base balance in hypercapnic catfish (Ictalurus nebulosus). Cell Tissue Res. 268, 539-552.
42. Hardisty, M. W. (1982). Lampreys and hagfishes: an analysis of cyclostome relationships. In The Biology of Lampreys, vol. 4B (ed. M. W. Hardisty and I. C. Potter), pp. 165-259. London: Academic Press.
43. Hardisty, M. W. and Potter, I. C. (1971). The general biology of adult lampreys. In The Biology of Lampreys, vol. 1 (ed. M. W. Hardisty and I. C. Potter), pp. 127-206. London: Academic Press.
44. Hardisty, M. W., Potter, I. C. and Milliard, R. W. (1989). Physiological adaptations of the living agnathans. Trans. Roy. Soc. Edinburgh Earth Sciences 80, 241-254.
45. Harris, H. W., Jr, Strange, K. and Zeidel, M. L. (1991). Current understanding of the cellular biolgy and molecular structure of the antidiuretic hormone-stimulated water transport pathway. J. Clin. Invest. 88, 1-8.
46. + pump in frog skin. Pflügers Arch. 406, 362-366.
47. + conductances and transport in frog skin epithelium. J. Gen. Physiol. 92, 767-791.
48. Hatae, T. and Benedetti, E. L. (1982). Mosaic structure in the plasma membrane: spiral arrays of subunits in the cytoplasmic tubules of lamprey chloride cells. J. Cell Sci. 56, 441-452.
49. Hootman, S. R. and Philpott, C. W. (1980). Accessory cells in teleost branchial epithelium. Am. J. Physiol. 238, R199-R206.
50. Hunter, M., Horisberger, J.-D., Stanton, B. and Giebisch, G. (1987). The collecting tubule of Amphiuma. I. Electrophysiological characterisation. Am. J. Physiol. 253, F1263-F1272.
51. Janvier, P. (1999). Catching the first fish. Nature 402, 21-22.
52. Karnaky, K. J., Jr (1980). Ion-secreting epithelia: chloride cells in the head region of Fundulus heteroditus. Am. J. Physiol. 238, R185-R198.
53. Karnaky, K. J., Jr (1986). Structure and function of the chloride cell of Fundulus heteroclitus and other teleosts. Am. Zool. 26, 209-224.
54. Karnaky, K. J., Jr and Kinter, W. B. (1977). Killifish opercular skin: a flat epithelium with a high density of chloride cells. J. Exp. Zool. 199, 355-364.
55. Karnaky, K. J., Jr, Ernst, S. A. and Philpott, C. W. (1976a). Teleost chloride cell. I. Response of pupfish Cyprinodon variegatus gill Na, K-ATPase and chloride cell fine structure to various high salinity environments. J. Cell Biol. 70, 144-156.
56. Karnaky, K. J., Jr, Kinter, L. B., Kinter, W. B. and Stirling, C. E. (1976b). Teleost chloride cell. II. Autoradiographic localization of gill Na, K-ATPase in killifish Fundulus heteroditus adapted to low and high salinity environments. J. Cell Biol. 70, 157-177.
57. Karnaky, K. J., Jr, Degnan, K. J. and Zadunaisky, J. A. (1977). Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science 195, 203-205.
58. Keys, A. B. and Willmer, E. N. (1932). Chloride secreting cells in the gills of fishes with special reference to the common eel. J. Physiol. (Lond) 76, 368-378.
59. King, J. A. C., Abel, D. C. and DiBona, D. R. (1989). Effects of salinity on chloride cells in the euryhaline cyprinodontid fish Rivulus marmoratus. Cell Tissue Res. 257, 367-377.
60. Kirschner, L. B. (1977). The sodium chloride excreting cells in marine vertebrates. In Transport of Water and Ions in Animals (ed. B. L. Gupta, R. B. Moreton, J. L. Oschman and B. J. Wall), pp. 427-452. London, New York, San Francisco: Academic Press.
61. Kirschner, L. B. (1980). Comparison of vertebrate salt-excreting organs. Am. J. Physiol. 238, R219-R223.
62. Kirschner, L. B. (1983). Sodium chloride absorption across the body surface: frog skins and other epithelia. Am. J. Physiol. 244, R429-R443.
63. + secretion in turtle bladder. Am. J. Physiol. 272, F491-F497.
64. Krogh, A. (1939). Osmotic Regulation in Aquatic Animals. London: Cambridge University Press.
65. Kuraku, S., Hoshiyama, D., Katoh, K., Suga, H. and Miyata, T. (1999). Monophyly of lampreys and hagfishes supported by nuclear DNA-coded genes. J. Mol. Evol. 49, 729-735.
66. Lang, F. (1988). NaCl transport in the kidney. In Advances in Comparative and Environmental Physiology, vol. 1 (ed. R. Greger), pp. 153-188. Berlin, Heidelberg: Springer-Verlag.
67. Larsen, E. H. (1988). NaCl transport in amphibian skin. In Advances in Comparative and Enviromental Physiology, vol 1 (ed. R. Greger), pp. 189-248. Berlin, Heidelberg: Springer-Verlag.
68. Larsen, E. H. (1991). Chloride transport by high-resistance heterocellular epithelia. Physiol. Rev. 77, 235-283.
69. Larsen, E. H., Willumsen, N. J. and Christoffersen, B. C. (1992). Role of proton pump of mitochondria-rich cells for active transport of chloride ions in toad skin epithelium. J. Physiol. 450, 203-216.
70. Laurent, P. (1984). Gill internal morphology. In Fish Physiology, vol. 10, part A (ed. W. S. Hoar and D. J. Randall), pp. 73-183. Orlando: Academic Press.
71. Loretz, C. A. (1995). Electrophysiology of ion transport in teleost intestinal cells. In Cellular and Molecular Approaches to Fish Ionic Regulation (ed. C. M. Wood and T. J. Shuttleworth), pp. 25-56. Toronto: Academic Press.
72. Lutz, P. (1975). Adaptive and evolutionary aspects of the ionic content of fishes. Copeia 1975, 369-373.
73. Macknight, A. D. C., DiBona, D. R. and Leaf, A. (1980). Sodium transport across toad urinary bladder: a model tight epithelium. Physiol. Rev. 60, 615-715.
74. Mallatt, J. and Ridgway, R. L. (1984). Ultrastructure of a complex epithelial system: the pharyngeal lining of the larval lamprey Petromyzon marinus. J. Morphol. 180, 271-296.
75. Mallatt, J. and Sullivan, J. (1998). 28S and 18S rDNA sequences support the monophyly of lampreys and hagfishes. Mol. Biol. Evol. 15, 1706-1718.
76. Mallatt, J., Bailey, J. F., Lampa, S. J., Evans, M. A. and Tate, W. (1995). Quantitative ultrastructure of gill epithelial cells in the larval lamprey Petromyzon marinus. Can. J. Fish Aquat. Sci. 52, 1150-1164.
77. 2+ transport by fish gills: retrospective review and prospective synthesis. J. Exp. Zool. 293, 264-283.
78. Marshall, W. S., Bryson, S. E., Darling, P., Whitten, C., Patrick, M., Wilkie, M., Wood, C. M. and Buckland-Nicks, J. (1997). NaCl transport and ultrastructure of opercular epithelium from a freshwater-adapted euryhaline teleost, Fundulus heteroclitus. J. Exp. Zool. 277, 213-237.
79. Marshall, W. S., Lynch, E. M. and Cozzi, R. R. F. (2002). Redistribution of immunofluorescence of CFTR anion channel and NKCC cotransporter in chloride cells during adaptation of the killifish Fundulus heteroclitus to sea water. J. Exp. Biol. 205, 1265-1273.
80. McFarland, W. and Munz, F. W. (1965). Regulation of body weight and serum composition by hagfish in various media. Comp. Biochem. Physiol. 14, 383-398.
81. Morris, R. (1956). The osmoregulation ability of the lampern (Lampetra fluviatilis L.) in sea water during the course of its spawning migration. J. Exp. Biol. 23, 235-248.
82. Morris, R. (1957). Some aspects of the structure and cytology of the gills of Lampetra fluviatilis. Q. J. Microsc. Sci. 98, 473-485.
83. Morris, R. (1958). The mechanism of marine osmoregulation in the lampern (Lampetra fluviatilis L.) and the causes of its breakdown during the spawning migration. J. Exp. Biol. 35, 649-665.
84. Morris, R. (1972). Osmoregulation. In The Biology of Lampreys, vol. 2 (ed. W. M. Hardisty and I. C. Potter), pp. 192-239. London: Academic Press.
85. Morris, R. (1980). Blood composition and osmoregulation in ammocoete larva. Can. J. Fish Aquat. Sci. 37, 1665-1679.
86. Morris, R. and Pickering, A. D. (1975). Ultrastructure of presumed ion-transporting cells in the gills of ammocoete lampreys, Lampetra fluviatilis (L.) and Lampetra planeri (Bloch). Cell Tissue Res. 163, 327-341.
87. Morris, R. and Pickering, A. D. (1976). Changes in the ultrastructure of the gills of the river lamprey, Lampetra fluviatilis (L.), during the anadromous spawning migration. Cell Tissue Res. 173, 271-277.
88. Nagel, W. and Dörge, A. (1996). The role of mitochondria-rich cells in sodium transport across amphibian skin. Pflügers Arch. Eur. J. Physiol. 433, 146-152.
89. Nakao, T. (1974). Fine structure of the agranular cytoplasmic tubules in the lamprey chloride cells. Anat. Rec. 178, 49-62.
90. Parry, G. (1966). Osmotic adaptation in fishes. Biol. Rev. 41, 392-444.
91. Peek, W. D. and Youson, J. H. (1979a). Ultrastructure of chloride cells in young adults of the anadromous sea lamprey, Petromyzon marinus L., in fresh water and during adaptation to sea water. J. Morph. 160, 143-163.
92. Peek, W. D. and Youson, J. H. (1979b). Transformation of the interlamellar epithelium of the gills of the anadromous sea lamprey, Petromyzon marinus L., during metamorphosis. Can. J. Zool. 57, 1318-1332.
93. Perry, S. F. (1997). The chloride cell: structure and function in the gills of freshwater fishes. Annu. Rev. Physiol. 59, 325-347.
94. Philpott, C. W. and Copeland, D. E. (1963). Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18, 389-404.
95. Pickering, A. D. and Morris, R. (1970). Osmoregulation of Lampetra fluviatilis L. and Petromyzon marinus (Cyclostomata) in hyperosmotic solutions. J. Exp. Biol. 53, 231-243.
96. Pisam, M. and Rambourg, A. (1991). Mitochondria-rich cells in the gill epithelium of teleost fishes: an ultrastructural approach. Int. Rev. Cytol. 130, 191-232.
97. Philpott, C. W. (1966). The use of horseradish peroxidase to demonstrate functional continuity between the plasmalemma and the unique tubular system of the chloride cell. J. Cell Biol. 31, 86.
98. Potter, I. C. (1980). Ecology of larval and metamorphosing lampreys. Can. J. Fish. Aquat. Sci. 37, 1641-1657.
99. Potter, I. C. and Beamish, F. W. H. (1977). The freshwater biology of adult anadromous sea lampreys Petromyzon marinus. J. Zool. (Lond.) 181, 113-130.
100. Potter, I. C. and Hilliard, R. W. (1987). A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes). J. Zool. (Lond.) 212, 713-737.
101. Potter, I. C. and Huggins, R. J. (1973). Observations on the morphology, behaviour and salinity tolerance of downstream migrating river lamprey (Lampetra fluviatilis). J. Zool. (Lond.) 169, 365-379.
102. Potter, I. C., Hilliard, R. W. and Bird, D. J. (1980). Metamorphosis in the Southern Hemisphere lamprey, Geotria australis. J. Zool. (Lond.) 190, 405-430.
103. Potts, W. T. W. (1984). Transepithelial potential in fish gills. In Fish Physiology, vol. 10, part B (ed. W. S. Hoar and D. J. Randall), pp. 105-128. Orlando: Academic Press.
104. Rick, R., Dörge, A., v. Arnim, E. and Thurau, K. (1978). Electron microprobe analysis of frog skin epithelium: evidence for a syncytial sodium transport compartment. J. Membr. Biol. 39, 313-331.
105. Riddle, C. V. and Ernst, S. A. (1979). Structural simplicity of the zonula occludens in the electrolyte secreting epithelium of the avian salt gland. J. Memhr. Biol. 45, 21-35.
106. Robertson, J. D. (1957). The habitat of the early vertebrates. Biol. Rev. 32, 156-187.
107. Robertson, J. D. (1974). Osmotic and ionic regulation in cyclostomes. In Chemical Zoology, vol. 8 (ed. M. Florkin and B. T. Scheer), pp. 149-193. New York: Academic Press.
108. Sardet, C. (1980). Freeze-fracture of the gill epithelium of euryhaline teleost fishes. Am. J. Physiol. 238, R207-R212.
109. Sardet, C., Pisam, M. and Maetz, J. (1979). The surface epithelium of teleostean fish gills. Cellular and junctional adaptations of the chloride cell in relation to salt adaptation. J. Cell Biol. 80, 96-117.
110. Shu, D.-G., Luo, H.-L., Conway Morris, S., Zhang, X.-L., Hu, S.-X., Chen, L., Zhu, M., Li, Y. and Chen, L.-Z. (1999). Lower Cambrian vertebrates from south China. Nature 402, 42-46.
111. Singer, T. D., Tucker, S. J., Marshall, W. S. and Higgins, C. F. (1998). A divergent CFTR homologue: highly regulated salt transport in the euryhaline teleost F. heteroclitus. Am. J. Physiol. 274, C715-C723.
112. Smith, H. W. (1930). The absorption and excretion of water and salts by marine teleosts. Am. J. Physiol. 93, 485-505.
113. Smith, H. W. (1932). Water regulation and its evolution in the fishes. Q. Rev. Biol. 7, 1-26.
114. 2 stimulation of proton secretion by turtle bladder. Am. J. Physiol. 245, C113-C120.
115. Stetson, D. L. and Steinmetz, P. R. (1985). α and β types of carbonic anhydrase-rich cells in turtle bladder. Am. J. Physiol. 249, F553-F565.
116. 2 stimulation in turtle bladder. Pflügers Arch. 407, S80-S84.
117. Stock, D. W. and Whitt, G. S. (1992). Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group. Science 257, 787-789.
118. +-ATPase) in pavement cells of rainbow trout gill. J. Exp. Biol. 198, 2619-2629.
119. Wade, J. B. (1976). Membrane structural specializations of the toad urinary bladder revealed by the freeze-fracture technique. II. The mitochondria-rich cell. J. Membr. Biol. 29, 111-126.
120. Wade, J. B., Di Scala, V. A. and Karnovsky, M. J. (1975). Membrane structural specialization of the toad urinary bladder revealed by the freeze fracture technique. I. The granular cell. J. Memhr. Biol. 22, 385-402.
121. Wade, J. B., Stetson, D. L. and Lewis, S. A. (1981). ADH action: evidence for a membrane shuttle mechanism. Ann. N.Y. Acacl. Sci. 372, 106-117.
122. Wilson, J. M. and Laurent, P. (2002). Fish gill morphology: inside out. J. Exp. Zool. 293, 192-213.
123. Wilson, J. M., Laurent, P., Tufts, B. L., Benos, D. J., Donowitz, M., Vogl, A. W. and Randall, D. J. (2000a). NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J. Exp. Biol. 203, 2279-2296.
124. Wilson, J. M., Randall, D. J., Donowitz, M., Vogl, A. W. and Ip, Y. K. (2000b). Immunolocalisation of ion-transport proteins to branchial epithelium mitochondria-rich cells in the mudskipper (Periophthalmodon schlosseri). J. Exp. Biol. 203, 2297-2310.
125. Youson, J. H. (1981). The alimentary canal. In The biology of Lampreys, vol. 3 (ed. M. W. Hardisty and I. C. Potter), pp. 95-189. London: Academic Press.
126. Youson, J. H. and Freeman, P. A. (1976). Morphology of the gills of larval and parasitic adult sea lamprey, Petromyzon marinus L. J. Morphol. 149, 73-104.
127. Zadunaisky, J. A. (1984). The chloride cell: the active transport of chloride and the paracellular pathways. In Fish Physiology, vol. 10B (ed. W. S. Hoar and D. J. Randall), pp. 130-176. Orlando: Academic Press.