Abstract
Morphological features of the gill and opercular epithelia of tilapia (Oreochromis mossambicus) have been compared in fish acclimated to either fresh water (FW) or hypersaline water (60‰ S) by scanning electron and fluorescence microscopy. In hyperosmoregulating, i.e., FW-acclimated, tilapia only those mitochondria-rich (MR) cells present on the filament epithelium of the gill were exposed to the external medium. After acclimation of fish to hypersaline water these cells become more numerous, hypertrophy extensively, and form apical crypts not only in the gill filament but also in the opercular epithelium. Regardless of salinity, MR cells were never found to be exposed to the external medium on the secondary lamellae. In addition, two types of pavement cells were identified having distinct morphologies, which were unaffected by salinity. The gill filaments and the inner operculum were generally found to be covered by pavement cells with microridges, whereas the secondary lamellae were covered exclusively by smooth pavement cells.
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Avella M, Masoni A, Bornancin M, Mayer-Gostan N (1987) Gill morphology and sodium influx in the rainbow trout (Salmo gairdneri) acclimated to artificial freshwater environments. J Exp Zool 241: 159–169
Bailly Y, Dunel-Erb S, Geffard M, Laurent P (1989) The vascular and epithelial serotonergic innervation of the actinopterygian gill filament with special reference to the trout, Salmo gairdneri. Cell Tissue Res 258: 349–363
Bierther M (1970) Die Chloridzellen des Stichlings. Z Zellforsch 107: 421–446
Brown P (1992) Gill chloride cell surface-area is greater in fresh-water-adapted adult sea trout (Salmo trutta L.) than those adapted to sea water. J Fish Biol 40: 481–484
Burns J, Copeland DE (1950) Chloride excretion in the head region of Fundulus heteroclitus. Biol Bull 99: 381–385
Cioni C, De Merich D, Cataldi E, Cataudella S (1991) Fine structure of chloride cells in freshwater-and saltwater-adapted Oreochromis niloticus (Linnaeus) and Oreochromis mossambicus (Peters). J Fish Biol 39: 197–209
Copeland DE (1950) Adaptive behaviour of the chloride cell in the gill of Fundulus heteroclitus. J Morphol 87: 369–376
Crocker PA, Gotto M, De Boer JA, Holt GJ, Arnold CR (1985) Notes on the surface structure of the gill arch epithelium in juvenile red drum, Sciaenops ocellatus exposed to salt and fresh water. Copeia 2: 515–518
Dunel-Erb S, Laurent P (1980) Ultrastructure of marine teleost gill epithelia: SEM and TEM study of the chloride cell apical membrane. J Morphol 165: 175–186
Dunel-Erb S, Bailly Y, Laurent P (1982) Neuroepithelial cells in fish gill primary lamellae. J Appl Physiol 53: 1342–1353
Dunel-Erb S, Bailly Y, Laurent P (1989) Neurons controlling the gill vasculature in five species of teleosts. Cell Tissue Res 255: 567–573
Evans DH (1993) Osmotic and ionic regulation. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 315–341
Fishelson L (1980) Scanning and transmission electron microscopy of the squamose gill-filament epithelium from fresh-and seawater-adapted Tilapia. Environ Biol Fish 5: 161–165
Foskett JK, Scheffey (1982) The chloride cell: definitive identification as the salt-secretory cell in teleost. Science 215: 164–166
Foskett JK, Logsdon CD, Turner T, Machen TE, Bern HA (1981) Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. J Exp Biol 93: 209–224
Franklin CE (1990) Surface ultrastructural changes in the gills of sockeye salmon (Teleostei: Oncorhynuchs nerka) during seawater transfer: comparison of successful and unsuccessful seawater adaptation. J Morphol 206: 13–23
Gardaire E, Isaia J, Bornancin M (1991) Kinetics of potassium transport across trout gills. Comp Biochem Physiol [A] 99: 615–620
Getman HC (1950) Adaptive changes in the chloride cells of Anguilla rostrata. Biol Bull 99: 439–445
Girard JP, Payan P (1977) Kinetic analysis and partitioning of sodium and chloride influxes across the gills of sea water adapted trout. J Physiol (Lond) 267: 519–536
Girard JP, Payan P (1980) Ion exchanges through respiratory and choride cells in freshwater-and seawater-adapted teleosteans. Am J Physiol 238: R260-R268
Gonzalez RJ, McDonald DG (1992) The relationship between oxygen consumption and ion loss in a freshwater fish. J Exp Biol 163: 317–332
Goss GG, Laurent P, Perry SF (1992a). Evidence for a morphological component in acid-base regulation during environmental hypercapnia in the brown bullhead (Ictalurus nebulosus). Cell Tissue Res 268: 539–552
Goss GG, Perry SF, Wood CM, Laurent P (1992b) Mechanisms of ion and acid-base regulation at the gills of freshwater fish. J Exp Zool 263: 143–159
Hawkes JW (1974) The structure of fish skin. I. General organization. Cell Tissue Res 149: 147–158
Hossler FE, Ruby JR, McIlwain JD (1979) The gill arch of the mullet, Mugil cephalus. II. modification in surface ultrastructure and Na-K-ATPase content during adaptation to various salinities. J Exp Zool 208: 399–406
Hossler FE, Musil G, Karnaky KJ Jr, Epstein FH (1985) Surface ultrastructure of the gill arch of the killifish, Fundulus heteroclitus, from seawater and freshwater, with special reference to the morphology of apical crypts of chloride cells. J Morphol 185:377–386
Hughes GM (1984) General anatomy of the gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10 A, Academic Press, New York, pp 1–72
Hughes GM, Morgan M (1973) The structure of the gills in relation to their respiratory function. Biol Rev 48:419–475
Hughes GM, Wright DE (1970) A comparative study of the ultrastructure of the water-blood pathway in the secondary lamellae of teleost and elasmobranch fishes: benthic forms. Z Zellforsch 104:478–493
Hwang PP (1987) Tolerance and ultrastructural responses of branchial chloride cells to salinity changes in the euryhaline teleost Oreochromis mossambicus. Marine Biol 94:643–649
Karnaky KJ Jr (1972) A system to study the teleost chloride cell with the Ussing chamber. Bull Mt Desert Isl Biol Lab 12:60–61
Karnaky KJ Jr, Kinter (1977) Killifish opercular skin: a flat epithelium with a high density of chloride cells. J Exp Zool 199:355–364
Kessel RG, Beams HW (1962) Electron microscope studies on the gill filament of Fundulus heteroclitus from sea water and fresh water with special reference to the ultrastructural organization of the “chloride cell”. J Ultrastruct Res 6:77–87
Kültz D, Jürss K (1993) Biochemical characterization of isolated branchial mitochondria-rich cells of Oreochromis mossambicus acclimated to freshwater or hyperhaline seawater. J Comp Physiol [B] 163:406–412
Kültz D, Onken H (1993) Long-term acclimation of the teleost Oreochromis mossambicus to various salinities: two different strategies in mastering hypertonic stress. Marine Biol 117:527–533
Laurent P (1985) A survey of the morpho-functional relationship between epithelia, vasculature and innervation within the fish gill. Fortschr Zool 30:339–351
Laurent P, Dunel S (1980) Morphology of gill epithelial in fish. Am J Physiol 238:R147-R159
Laurent P, Hebibi N (1989) Gill morphometry and fish osmoregulation. Can J Zool 67:3055–3063
Laurent P, Perry SF (1990) Effects of cortisol on gill chloride cell morphology and ionic uptake in the freshwater trout, Salmo gairdneri. Cell Tissue Res 259:429–442
Lubin RT, Rourke AW, Bradley TM (1989) Ultrastructural alterations in branchial chloride cells of Atlantic salmon, Salmo salar, during parr-smolt transformation and early development in sea water. J Fish Biol 34:259–272
Lubin RT, Rourke AW, Saunders RL (1991) Influence of photoperiod on the number and ultrastructure of gill chloride cells of the Atlantic salmon (Salmo salar) before and during smoltification. Can J Fish Aquat Sci 48:1302–1307
Maina JN (1990) A study of the morphology of the gills of an extreme alkalinity and hyperosmotic adapted teleost Oreochromis alcalicus grahami (Boulenger) with particular emphasis on the ultrastructure of the chloride cells and their modifications with water dilution: a SEM and TEM study. Anat Embryol 181:83–98
Maina JN (1991) A morphometric analysis of chloride cells in the gills of the teleosts Oreochromis alcalicus and Oreochromis niloticus and a description of presumptive urea excreting cells in O. alcalicus. J Anat 175:131–145
Marshall WS (1977) Transepithelial potential and short-circuit current across the isolated skin of Gillichthys mirabilis (Teleostei: Gobiidae), acclimated to 5% and 100% seawater. J Comp Physiol [B] 114:157–165
McDonald DG, Cavdek V, Ellis R (1991) Gill design in freshwater fishes: interrelationships among gas exchange, ion regulation, and acid-base regulation. Physiol Zool 64:103–123
Olson KR, Fromm PO (1973) A scanning electron microscopic study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z Zellforsch Mikrosk Anat 143:439–449
Pequeux A, Gilles R, Marshall WS (1988) NaCl transport in gills and related structures. In: Greger R (ed) Advances in comparative and environmental physiology, vol 1. Springer Berlin Heidelberg, pp 1–73
Philpott CW, Copeland DE (1963) Fine structure of chloride cells from three species of Fundulus. J Cell Biol 18:389–404
Pisam M, Rambourg A (1991) Mitochondria-rich cells in the gill epithelium of teleost fishes: an ultrastructural approach. Int Rev Cytol 130:191–232
Pisam M, Sardet C, Maetz J (1980) Polysaccharidic material in chloride cell of teleostean gill: modifications according to salinity. Am J Physiol 238:R213-R218
Randall DJ, Baumgarten D, Malyusz M (1972) The relationship between gas and ion transfer across the gills of fishes. Comp Biochem Physiol [A] 41:629–637
Sardet C, Pisam M, 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
Straus LP (1963) A study of the fine structure of the so-called chloride cell in the gill of the guppy Lebistes reticulatus P. Physiol Zool 36:183–198
Threadgold LT, Houston AH (1964) An electron microscope study of the “chloride cell” of Salmo salar L. Exp Cell Res 34:1–23
Weber E (1986) Grundriss der biologischen Statistik. 9 Aufl. Gustav Fischer, Jena
Whitear M (1990) Causative aspects of microridges on the surface of fish epithelia. J Submicrosc Cytol Pathol 22:211–220
Wilkie MP, Wood CM (1991) Nitrogenous waste excretion, acidbase regulation, and ionoregulation in rainbow trout (Oncorhynchus mykiss) exposed to extremely alkaline water. Physiol Zool 64:1069–1086
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Kültz, D., Jürss, K. & Jonas, L. Cellular and epithelial adjustments to altered salinity in the gill and opercular epithelium of a cichlid fish (Oreochromis mossambicus). Cell Tissue Res 279, 65–73 (1995). https://doi.org/10.1007/BF00300692
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DOI: https://doi.org/10.1007/BF00300692