Summary
The ultrastructure and density of chloride cells in the gill, opercular epithelium, and opercular skin of the euryhaline self-fertilizing fish Rivulus marmoratus (Cyprinodontidae) were studied with electron and fluorescence microscopy. R. marmoratus raised from birth in 1, 50, 100, and 200% seawater were compared. Chloride cells from fish raised in each of the four salinities exhibited an invaginated “pit” structure at the apical crypt. Multicellular complexes were present in the 1% seawater group and in those fish raised in higher salinities where elaborate interdigitations were seen between cells. Chloride cells from gills of fish raised in 200% seawater had a significantly higher percentage of their cytoplasmic volume composed of mitochondria than did those from fish raised in 1% seawater (69.9% vs 37.4%). The opercular skin and opercular epithelium had the same density of chloride cells (4.2×104-4.5×104 chloride cells/cm2), and this number did not vary significantly with increased salinity. The opercular skin thus appears far more responsive to environmental salinity than the opercular epithelium. Chloride cells from the opercular epithelium of fish raised in 200% seawater were found to be 39% larger than those from fish raised in 1% seawater, whereas the chloride cells from the opercular skin of the 200% seawater group were 107% larger than those from the 1% seawater group.
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References
Abel DC (1981) An ecological basis and adaptations for emergence in the cyprinodontid fish Rivulus marmoratus. MS thesis, College of Charleston, Charleston, South Carolina
Abel DC (1984) Terrestriality in the cyprinodontid fish Rivulus marmoratus: Potential utility in H2S and other bioassays. Bull Environ Contam Toxicol 33:33–39
Abel DC, Koenig CC, David WP (1987) Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environ Biol Fish 18:67–72
Bereiter-Hahn J (1976) Dimethylaminostyrylmethylpyridiniumiodine (DASPMI) as a fluorescent probe for mitochondria in situ. Biochim Biophys Acta 423:1–14
Brockman FW (1975) An unusual habitat for the fish Rivulus marmoratus. Florida Sci 38:35–36
Burns J, Copeland DE (1950) Chloride excretion in the head region of Fundulus heteroclitus. Biol Bull Mar Biol Lab Woods Hole 99:381–385
Butler DG, Carmichael FJ (1972) (Na+-K+)-ATPase activity in eel (Anguilla rostrata) gills in relation to changes in environmental salinity: Role of adrenocortical steroids. Gen Comp Endocrinol 19:421–427
Chretien M, Pisam M (1986) Cell renewal and differentiation in the gill epithelium of freshor salt-water-adapted euryhaline fish as revealed by (3H)-thymidine radioautography. Biol Cell 56:137–150
Copeland DE (1948) The cytological basis of chloride transfer in the gills of Fundulus heteroclitus. J Morphol 82:201–228
Copeland DE (1950) Adaptive behavior of the chloride cell in the gill of Fundulus heteroclitus. J Morphol 87:369–379
Courtney CM (1975) The production of organic detritus in an impounded mangrove forest. Ann Rep Marco Appl Mar Ecol Sta, July 1 1974–July 1, pp 197–232
Degnan KJ, Karnaky KJ Jr, Zadunaisky JA (1977) Active chloride transport in the in vitro opercular skin of a teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells. J Physiol (Lond) 271:155–191
Degnan KJ, Zadunaisky JA (1982) The opercular epithelium: An experimental model for teleost gill osmoregulation and chloride secretion. In: Zadunaisky JA (ed) Chloride Transport in Biological Membranes. Academic Press, New York, pp 295–318
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
Epstein FH, Katz AI, Pickford GE (1967) Sodium and potassiumactivated triphosphatase of gills: Role in adaptation of teleosts to salt water. Science 156:1245–1247
Epstein FH, Silva P, Kormanik G (1980) Role of Na-K-ATPase in chloride cell function. Am J Physiol 238 (Regul Integrative Comp Physiol 7):R246-R250
Ernst SA, Dodson WC, Karnaky KJ Jr (1980) Structural diversity of occluding junctions in the low resistance chloride-secreting opercular epithelium of seawater adapted killifish (Fundulus heteroclitus). J Cell Biol 87:488–497
Forrest JN, Cohen JRAD, Schon DA, Epstein FH (1973) Na transport and Na-K-ATPase in gills during adaptation to sea water: Effects of cortisol. Am J Physiol 224:709–713
Foskett JK, Logsdon CD, Turner T, Machen TE, Bern HA (1981) Differentiation of chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. J Exp Biol 93:209–224
Fujita M, Yamamoto T (1984) Selective demonstration by tannic acid of a special cytoplasmic tubular system in the chloride cells of teleost gills. Arch Histol Jp 47:113–118
Harrington RW Jr (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134:1749–1750
Harrington RW Jr (1963) Twenty-four-hour rhythms of internal self-fertilization and of oviposition by hermaphrodites of Rivulus marmoratus. Physiol Zool 36(4): 325–341
Harrington RW Jr, Kallman KD (1968) The homozygosity of clones of the self-fertilizing hermaphroditic fish Rivulus marmoratus Poey (Cyprinodontidae, Atheriniformes). Am Nat 102:337–343
Harrington RW Jr, Rivas LR (1958) The discovery in Florida of the cyprinodont fish, Rivulus marmoratus, with a redescription and ecological notes. Copeia 1958(2):125–130
Hastings RW (1969) Rivulus marmoratus from the west coast of Florida. Quart J Fla Acad Sci 32:37–38
Hootman SR, Philpott CW (1979) Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from the gills of a euryhaline teleost. Anat Rec 193:99–130
Hootman SR, Philpott CW (1980) Accessory cells in teleost branchial epithelium. Am J Physiol 238 (Regul Integrative Comp Physiol 7):R199-R206
Hossler FE (1980) Gill arch of the mullet, Mugil cephalus III. Rate of response to salinity change. Am J Physiol 238 (Regul Integrative Comp Physiol 7):R160-R164
Hossler FE, Harpole JH Jr, King JA (1986) The gill arch of the striped bass, Morone saxatilis I. Surface ultrastructure. J Submicrosc Cytol 18:519–528
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
Hossler FE, Ruby JR, McIlwain TD (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
Huehner MK, Schramm ME, Hens MD (1985) Notes on the behavior and ecology of the killifish Rivulus marmoratus Poey 1880 (Cyprinodontidae). Florida Sci 48:1–7
Hwang PP (1987) Tolerance and ultrastructural responses of branchial chloride cells to salinity changes in the teleost Oreochromis mossambicus. Marine Biol 94:643–649
Hwang PP (1988) Multicullular complex of chloride cells in the gills of freshwater teleosts. J Morphol 196:15–22
Hwang PP, Hirano R (1985) Effects of environmental salinity on intercellular organization and junctional structure of chloride cells in early stages of teleost development. J Exp Zool 236:115–126
Kallman KD, Harrington RW Jr (1964) Evidence for the existence of homozygous clones in the self-fertilizing hermaphroditic teleost Rivulus marmoratus (Poey). Biol Bull 126:101–114
Kamiya M, Utida S (1968) Changes in activity of sodium-potassium-activated adenosinetriphosphatase in gill during adaptation of the Japanese eel to sea water. Comp Biochem Physiol 26:675–685
Karnaky KJ Jr (1980) Ion-secreting epithelia: Chloride cells in the head region of Fundulus heteroclitus. Am J Physiol 238 (Regul Integrative Comp Physiol 7):R185-R198
Karnaky KJ Jr (1986) Structure and function of the chloride cell of Fundulus heteroclitus and other teleosts. Am Zool 26:209–224
Karnaky KJ Jr, Kinter WB (1977) Killifish opercular skin: A flat epithelium with a high density of chloride cells. J Exp Zool 199:355–364
Karnaky KJ Jr, Ernst SA, Philpott CW (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
Karnaky KJ Jr, Kinter LB, Kinter WB, Stirling CE (1976b) Teleost chloride cell II. Autoradiographic localization of gill Na, KATPase in killifish Fundulus heteroclitus adapted to low and high salinity environments. J Cell Biol 70:157–177
Karnaky KJ Jr, Degnan KJ, Zadunaisky JA (1977) Chloride transport across the isolated opercular epithelium of killifish: A membrane rich in chloride cells. Science 195:203–205
Karnaky KJ Jr, Degnan KJ, Zadunaisky JA (1979) Correlation of chloride cell number and short-circuit current in chloride-secreting epithelia of Fundulus heteroclitus. Bull Mt Desert Isl Biol Lab 19:109–111
Karnaky KJ Jr, Degnan KJ, Garretson LT, Zadunaisky JA (1984) Identification and quantification of mitochondria-rich cells in transporting epithelia. Am J Physiol 246 (Regul Integrative Comp Physiol 15):R770-R775
Kessel RG, Beams HW (1962) Electron microscope studies on the gill filaments 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
Keys A, Willmer EN (1932) “Chloride secreting cells” in the gills of fishes, with special reference to the common eel. J Physiol 76:368–378
Lacy ER (1983) Histochemical and biochemical studies of carbonic anhydrase activity in the opercular epithelium of the euryhaline teleost, Fundulus heteroclitus. Am J Anat 166:19–39
Laurent P, Dunel S (1980) Morphology of gill epithelia in fish. Am J Physiol 238 (Regul Integrative Comp Physiol 7):R147-R159
Marshall WS, Nishioka RS (1980) Relation of mitochondria-rich chloride cells to active chloride transport in the skin of a marine teleost. J Exp Zool 214:147–156
Mashiko K (1977) Metabolism of salt. In: Kawamoto NY (ed) Fish Physiology. Kosheisha Kosheikaku Co, pp 354–370 (in Japanese)
Nonnotte G, Nonnotte K, Kirsch R (1979) Chloride cells and chloride exchange in the skin of a sea-water teleost, the shanny (Blennius pholis L). Cell Tissue Res 199:387–396
Philpott CW (1962) Comparative morphology of the chloride secreting cells of three species of Fundulus as revealed by the electron microscope. Anat Rec 142:267–268
Philpott CW, Copeland DE (1963) Fine structure of chloride cells from three species of Fundulus. J Cell Biol 18:389–404
Pisam M (1981) Membranous systems in the “chloride cell” of teleostean fish gill: Their modifications in response to the salinity of the environment. Anat Rec 200:401–414
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
Sargent JR, Thomson AJ (1974) The nature and properties of the inducible sodium-plus-potassium ion dependent adenosine triphosphatase in the gills of eels (Anguilla anguilla) adapted to fresh water and sea water. Biochem J 144:69–75
Schwerdtfeger WK, Bereiter-Hahn J (1978) Transient occurrence of chloride cells in the abdominal epidermis of the guppy, Poecilia reticulata Peters, adapted to sea water. Cell Tissue Res 191:463–471
Shirai N (1972) Electron-microscope localization of sodium ions and adenosinetriphosphatase in chloride cells of the Japanese eel Anguilla japonica. J Fac Sci Univ Tokyo Sect 4 12(3): 385–403
Shirai N, Utida S (1970) Development and degeneration of the chloride cell during seawater and freshwater adaptation of the Japanese eel, Anguilla japonica. Z Zellforsch Mikrosk Anat 103:247–264
Silva P, Solomon R, Spokes K, Epstein FH (1977) Ouabain inhibition of gill Na-K-ATPase: Relationship to active chloride transport. J Exp Zool 199:419–426
Sokal RR, Rohlf FJ (1973) In: Introduction to Biostatistics. WH Freeman and Company, San Francisco, pp 13–14, 215–217
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
Tay K-L, Garside ET (1979) Adaptive hyperplasia of epidermal chloride-secreting cells in fry of mummichog, Fundulus heteroclitus L., incubated and reared in supranormal salinity. Can J Zool 57:1803–1807
Thomerson JE (1966) Rivulus marmoratus, a rare and unusual killifish from Florida. J Am Killifish Assoc 3:48–51
Thomson AJ, Sargent JR (1977) Changes in the levels of chloride cells and (Na++K+)-dependent ATPase in the gills of yellow and silver eels adapting to seawater. J Exp Zool 200:33–40
Utida S, Kamiya M, Shirai N (1971) Relationship between the activity of Na-K-activated adenosinetriphosphatase and the number of chloride cells in eel gills with special reference to seawater adaptation. Comp Biochem Physiol 38A:443–448
Vrijenhoek RC (1985) Homozygosity and interstrain variation in the self-fertilizing hermaphroditic fish, Rivulus marmoratus. J Hered 76:82–84
Weibel ER, Bolender RP (1973) Stereological techniques for electron microscopic morphometry. In: Hayat MA (ed) Principles and Techniques of Electron Microscopy. Vol. 3. Van Nostrand Reinhold, New York, pp 237–296
Zadunaisky JA (1984) The chloride cell: The active transport of chloride and the paracellular pathways. In: Hoar WS, Randall DJ (eds) Fish Physiology. Vol XB. Academic Press, Orlando, Florida, pp 129–176
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King, J.A.C., Abel, D.C. & DiBona, D.R. Effects of salinity on chloride cells in the euryhaline cyprinodontid fish Rivulus marmoratus . Cell Tissue Res. 257, 367–377 (1989). https://doi.org/10.1007/BF00261839
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DOI: https://doi.org/10.1007/BF00261839