Skip to main content
SpringerLink
Log in

Ion balance, acid-base regulation, and chloride cell function in the common killifish,Fundulus heteroclitus—a euryhaline estuarine teleost

  • Published:
Estuaries Aims and scope Submit manuscript

Abstract

The common killifish,Fundulus heteroclitus, is a euryhaline teleost common throughout estuaries of eastern North America. This symposium paper reviews the important contributions of the killifish to our present understanding of ionoregulation in seawater (SW) fish and their mechanisms of euryhalinity, and presents new data developing the killifish as a freshwater (FW) model system. Experiments on killifish have characterized (i) drinking in SW and its reduction in FW; (ii) the adaptive roles of the kidney to SW and FW conditions; (iii) the instantaneous (Phase I) and delayed (Phase II) reductions in Na+ outflux that occur upon transfer from SW to FW; (iv) the importance of prolactin secretion in the Phase II effect; (v) the cortisol-stimulated induction of branchial Na+, K+-ATPase that occurs upon transfer from FW to SW; (vi) the accompanying changes in morphology of the mitochondria-rich (MR) or “chloride cells” on the gills; (vii) the localization of this Na+, K+-ATPase activity to the basolateral membrane of chloride cells; and (viii) the NaCl-secretory function of these cells in SW. The opercular epithelium, which is rich in chloride cells, has been used as an in vitro model to characterize the mechanisms and control of NaCl secretion in SW fish. Much less is known about gill function in fresh water (inward NaCl transport), primarily due to the absence of a comparable freshwater model. Here we show that killifish acclimated to dilute FW ([NaCl] = 1 mmol I−1) possess large numbers of MR cells on the opercular epithelium. When mounted in vitro with FW on the outside, the preparation develops a large inside negative transepithelial potential (TEP) that is a Na+ diffusion potential. By the Ussing flux ratio criterion, Na+ fluxes are passive, but a small active influx of Cl− occurs, an observation that supports the involvement of MR cells in active Cl− uptake. This FW opercular epithelium if bathed with isotonic saline on both sides does not secrete Cl−, indicating that the MR cells indeed are of the FW type. In vivo, the fish exhibits a high rate of Na+ influx and outflux; Cl− outflux is much lower, and there is no detectable Cl− influx. Experimental variation of FW [NaCl] reveals a saturable, low affinity Na+ uptake mechanism, a Cl− influx mechanism that is activated only at much higher concentrations, and no evidence of exchange diffusion. Acid-base disturbance appears to be corrected by differential regulation of the outflux components only. Hence, the FW killifish ionoregulates somewhat differently from the few other FW teleosts that have been examined, and its opercular epithelium will serve as a very useful model system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  • Atz, J. W. 1986.Fundulus heteroclitus in the laboratory: A history.American Zoologist 26:111–120.

    Google Scholar 

  • Avella, M. andM. Bornancin. 1989. A new analysis of ammonia and sodium transport through the gills of the fresh-water rainbow trout (Salmo gairdner).Journal of Experimental Biology 142:155–175.

    Google Scholar 

  • Bereiter-Hahn, J. 1976. Dimethylaminostyrylmethylpyridiniumiodine (DASPMI) as a fluorescent probe for mitochondria in situ.Biochimica et Biophysica Acta 423:1–14.

    Article  CAS  Google Scholar 

  • Bern, H. A. andS. S. Madsen 1992. A selective survey of the endocrine system of the rainbow trout (Oncorhynchus mykiss) with emphasis on the hormonal regulation of ion balance.Aquaculture 100:237–262.

    Article  CAS  Google Scholar 

  • Bevelander, G. 1935. A comparative study of the branchial epithelium in fishes, with special reference to extrarenal excretion.Journal of Morphology 57:335–352.

    Article  Google Scholar 

  • Bevelander, G. 1936. Branchial glands in fishes.Journal of Morphology 59:215–224.

    Article  Google Scholar 

  • Bornancin, M., S. DeRenzis, andJ. Maetz. 1977. Branchial Cl− transport, anion stimulated ATPase, and acid-base balance inAnguilla anguilla adapted to freshwater: Effects of hyperoxia.Journal of Comparative Physiology 117:313–322.

    CAS  Google Scholar 

  • Burden, C. E. 1956. The failure of, hypophysectionizedFundulus heteroclitus to survive in fresh water.Biological Bulletin 110:8–28.

    Article  CAS  Google Scholar 

  • Burns, J. andD. E. Copeland. 1950. Chloride excretion in the head region ofFundulus heteroclitus.Biological Bulletin 99:381–385.

    Article  CAS  Google Scholar 

  • Copeland, D. E. 1948. The cytological basis of chloride transfer in the gills ofFundulus heteroclitus.Journal of Morphology 82: 201–227.

    Article  CAS  Google Scholar 

  • Copeland, D. E. 1950. Adaptive behaviour of the chloride cell in the gill ofFundulus heteroclitus.Journal of Morphology 87:369–379.

    Article  CAS  Google Scholar 

  • Degnan, K. J. 1984. Sodium and chloride dependence of chloride secretion by the opercular epithelium.Journal of Experimental Zoology 231:11–17.

    Article  CAS  Google Scholar 

  • Degnan, K. J. 1985. The role of K+ and Cl− conductances in chloride secretion by opercular epithelium.Journal of Experimental Zoology 236:19–31.

    Article  CAS  Google Scholar 

  • Degnan, K. J., K. J. Karnaky, andJ. A. Zadunaisky. 1977. Active chloride transport in the in vitro opercular skin of a teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells.Journal of Physiology 271:155–191.

    CAS  Google Scholar 

  • Degnan, K. J. andJ. A. Zadunaisky. 1979. Open-circuit Na+ and Cl− fluxes across isolated opercular epithelium from the teleostFundulus heteroclitus.Journal of Physiology 294:483–495.

    CAS  Google Scholar 

  • Degnan, K. J. andJ. A. Zadunaisky. 1980a. Ionic contributions to the potential and current across the opercular epithelium.American Journal of Physiology 238:R231-R239.

    CAS  Google Scholar 

  • Degnan, K. J. andJ. A. Zadunaisky. 1980b. Passive sodium movements across the opercular epithelium: The paracellular shunt pathway and ionic conductance.Journal of Membrane Biology 55:175–185.

    Article  CAS  Google Scholar 

  • Denoncourt, R. F., J. C. Fisher andK. M. Rapp. 1978. A freshwater population of the mummichog,Fundulus heteroclitus, from the Susquehanna River drainage in Pennsylvania.Estuaries 1:269–272.

    Article  Google Scholar 

  • DiMichelf, L. andM. H. Taylor. 1980. The environmental control of hatching inFundulus heteroclitus.Journal of Experimental Zoology 214:181–187.

    Article  Google Scholar 

  • Doyle, W. L. andD. Gorecki. 1961. The so-called chloride cell of the fish gill.Physiological Zoology 34:81–85.

    Google Scholar 

  • Dunson, W. A. andJ. Travis. 1994. Patterns in the evolution of physiological specializations in salt marsh animals.Estuaries 17:102–110.

    Article  Google Scholar 

  • Ehrenfeld, J., F. Garcia-Romeu, andB. J. Harvey. 1985. Electrogenic active proton pump inRana esculenta skin and its role in sodium ion transport.Journal of Physiology 359:331–355.

    CAS  Google Scholar 

  • Epstein, F., A. I. Katz, andG. E. Pickford. 1967. Sodium and potassium-activated adenosine triphosphatase of gills: Role in adaptation of teleosts to salt water.Science 156:1245–1247.

    Article  CAS  Google Scholar 

  • Epstein, F. H., A. Manitius, E. Weinstein, A. I. Katz andG. E. Pickford. 1969. Sodium and potassium activated adenosine triphosphatase in kidneys ofFundulus heteroclitus adapted to fresh and salt water.Yale Journal of Biology and Medicine 41:388–393.

    CAS  Google Scholar 

  • Eriksson, O., N. Mayer-Gostan, andP. J. Wistrand. 1985. The use of isolated fish opercular epithelium as a model tissue for studying intrinsic activities of loop diuretics.Acta Physiological Scandinavica 125:55–66.

    CAS  Google Scholar 

  • Ernst, S. A., W. C. Dodson, andK. J. Karnaky. 1980. Structural diversity of occluding junctions in the low resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus).Journal of Cell Biology 87:488–497.

    Article  CAS  Google Scholar 

  • Evans, D. H., J. B. Claiborne, L. Farmer, C. Mallery, andE. J. Krasny. 1982. Fish gill ionic transport: Methods and models.Biological Bulletin 163:108–130.

    Article  CAS  Google Scholar 

  • Finn, A. L. andJ. Bright. 1978. The paracellular pathway in toad urinary bladder: Permselectivity and kinetics of opening.Journal of Membrane Biology 44:67–83.

    Article  CAS  Google Scholar 

  • Fleming, W. R. andF. I. Kamemoto. 1963. The site of sodium outflux from the gill ofFundulus kansae.Comparative Biochemistry and Physiology 8:263–269.

    Article  Google Scholar 

  • Fleming, W. R. andJ. G. Stanley. 1965. Effects of rapid changes in salinity on the renal function of a euryhaline teleost.American Journal of Physiology 209:1025–1030.

    CAS  Google Scholar 

  • Forrest, J. N., Jr.,A. D. Cohen, D. A. Schon, andF. H. Epstein. 1973a. Na transport and Na-K-ATPase in gills during adaptation to seawater: Effects of cortisol.American Journal of Physiology 224:709–713.

    CAS  Google Scholar 

  • Forrest, J. N., Jr.,W. C. MacKay, B. Gallagher, andF. H. Epstein. 1973b. Plasma cortisol response to saltwater adaptation in the American eel,Anguilla rostrata.American Journal of Physiology 224:714–717.

    CAS  Google Scholar 

  • Foskett, J. K., H. A. Bern, T. E. Machen, andM. Conner. 1983. Chloride cells and the hormonal control of teleost fish osmoregulation.Journal of Experimental Biology 106:255–281.

    CAS  Google Scholar 

  • Foskett, J. K., D. Logsdon, T. Turner, T. E. Machen, andH. A. Bern. 1981. Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlidSarotherodon mossambicus.Journal of Experimental Biology 93:209–224.

    Google Scholar 

  • Foskett, J. K. andT. E. Machen. 1985. Vibrating probe analysis of teleost opercular epithelium: Correlation between active transport and leak pathways of individual chloride cells.Journal of Membrane Biology 85:23–35.

    Google Scholar 

  • Foskett, J. K., T. E. Machen, andH. A. Bern. 1982. Chloride secretion and conductance of teleost opercular membrane: Effects of prolactin.American Journal of Physiology 242:R380-R389.

    CAS  Google Scholar 

  • Foskett, J. K. andC. Scheffey 1982. The chloride cell: Definitive identification as the salt secretory cell in teleosts.Science 215:164–165.

    Article  CAS  Google Scholar 

  • Frizzell, R. A., M. Field, andS. G. Schutz. 1979. Sodiumcoupled chloride transport by epithelial tissues.American Journal of Physiology 236:F1-F8.

    CAS  Google Scholar 

  • Garcia-Romeu, F. andR. Motais. 1966. Mise en evidence d’échange Na+/NH4 + chez l’anguille de’eau douce.Comparative Biochemistry and Physiology 17:1201–1204.

    Article  Google Scholar 

  • Goss, G. G., P. L. Laurent andS. F.Perry. 1992a. Evidence for a morphological component in acid-base regulation during environmental hypercapnia in the brown bullhead,Ictalurus nebulosus.Cell and Tissue Research 268:539–552.

    Article  CAS  Google Scholar 

  • Goss, G. G., S. F. Perry, C. M. Wood, andP. L. Laurent. 1992b. Mechanisms of ion and acid-base regulation at the gills of freshwater fish.Journal of Experimental Zoology 263: 143–159.

    Article  CAS  Google Scholar 

  • Goss, G. G. andC. M. Wood. 1991. Two-substrate kinetic analysis: A novel approach linking ion and acid-base transport at the gills of the freshwater troutOncorhynchus mykiss.Journal of Comparative Physiology B 161:635–646.

    Article  CAS  Google Scholar 

  • Grau, E. G., P. Prunet, T. Gross, R. S. Nishioka, andH. A. Bern. 1984. Bioassay for salmon prolactin using hypophysectionizedFundulus heteroclitus.General and Comparative Endocrinology 53:78–85.

    Article  CAS  Google Scholar 

  • Griffith, R. W. 1974. Environmental and salinity tolerance in the genusFundulus.Copeia 1974:319–331.

    Article  Google Scholar 

  • Guggino, W. B. 1980. Salt balance in embryos ofFundulus heteroclitus andF. bermudae adapted to seawater.American Journal of Physiology 238:R42-R49.

    CAS  Google Scholar 

  • Hasegawa, S., T. Hirano, andH. Kawauchi. 1986. Sodium-retaining activity of chum salmon prolactin in some euryhaline teleosts.General and Comparative Endocrinology 63:309–317.

    Article  CAS  Google Scholar 

  • Heisler, N. 1982. Transepithelial ion transfer processes as mechanisms for fish acid-base regulation in hypercapnia and lactacidosis.Canadian Journal of Zoology 60:1108–1122.

    Article  CAS  Google Scholar 

  • Heisler, N. 1984. Acid-base regulation in fishes, p. 315–401.In D. J. Randall and W. S. Hoar (eds.), Fish Physiology, Vol. 10A. Academic Press, Orlando, Florida.

    Google Scholar 

  • Hirano, T. 1986. The spectrum of prolactin action in teleosts, p. 53–74.In C. L. Ralph (ed.), Comparative Endocrinology: Developments and Directions. Alan R. Liss, New York.

    Google Scholar 

  • Hootman, S. R. andC. W. Philpott. 1974. Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from the gills of a euryhaline teleost.Anatomical Record 193: 99–129.

    Article  Google Scholar 

  • Hootman, S. R. andC. W. Philpott. 1980. Accessory cells in teleost branchial epithelium.American Journal of Physiology 238:R185-R198.

    Google Scholar 

  • Hyde, D. A. andS. F. Perry. 1987. Acid-base, and ionic regulation in the American eel (Anguilla rostrata) during and after prolonged aerial exposure: Branchial and renal adjustment.Journal of Experimental Biology 133:429–447.

    Google Scholar 

  • Jacob, W. F. andM. H. Taylor. 1983. The time course of seawater acclimation inFundulus heteroclitus L.Journal of Experimental Zoology 228:33–39.

    Article  CAS  Google Scholar 

  • Karnaky, K. J. 1980. Ion-secreting epithelia: Chloride cells in the head region ofFundulus heteroclitus.American Journal of Physiology 238:R185-R198.

    CAS  Google Scholar 

  • Karnaky, R. J. 1986. Structure and function of the chloride cell ofFundulus heteroclitus and other teleosts.American Zoologist 26:209–224.

    CAS  Google Scholar 

  • Karnaky, K. J. K. J. Degnan, L. T. Garretson, andJ. A. Zadunaisky. 1984. Identification and quantification of mitochondria-rich cells in transporting epithelia.American Journal of Physiology 246:R770-R775.

    CAS  Google Scholar 

  • Karnaky, K. J., K. J. Degnan, andJ. A. Zadunaisky. 1977. Chloride transport across isolated opercular epithelium of killifish: A membrane rich in chloride cells.Science 195:203–205.

    Article  CAS  Google Scholar 

  • Karnaky, K. J. andW. B. Kinter. 1977. Killifish opercular skin: A flat epithelium with a high density of chloride cells.Journal of Experimental Zoology 199:355–364.

    Article  Google Scholar 

  • Karnaky, K. J. L. B. Kinter, W. B. Kinter, andC. E. Stirling. 1976. Teleost chloride cell. II. Auto-radiographic localization of gill Na,K-ATPase in killifish (Fundulus heteroclitus) adapted to low and high salinity environments.Journal of Cell Biology 70:157–177.

    Article  CAS  Google Scholar 

  • Kerstetter, T. H. andL. B. Kirschner. 1974. HCO3 −-dependent ATPase activity in the gills of rainbow trout (Salmo gairdneri).Comparative Biochemistry and Physiology 488:581–589.

    Google Scholar 

  • Keys, A. B. andE. N. Willmer. 1932. Chloride secretory cells in the gills of fishes with special references to the common eel.Journal of Physiology 76:368–377.

    CAS  Google Scholar 

  • Klyce, S. D. andC. E. 1985. Transport processes across the rabbit corneal epithelium: A review.Current Eye Research 4:323–331.

    Article  CAS  Google Scholar 

  • Klyce, S. D. andR. K. S. Wong. 1977. Site and mode of adrenaline action on chloride transport across the rabbit corneal epithelium.Journal of Physiology 266:777–799.

    CAS  Google Scholar 

  • Kneib, R. T. 1986. The role ofFundulus heteroclitus in salt marsh trophic dynamics.American Zoologist 26:259–269.

    Google Scholar 

  • Lacy, E. R. 1983. Histochemical and biochemical studies of carbonic anhydrase activity in the opercular epithelium of the euryhaline teleostFundulus heteroclitus.American Journal of Anatomy 166:19–39.

    Article  CAS  Google Scholar 

  • Lin, H. andD. Randall. 1991. Evidence for the presence of an electrogenic proton pump on the trout gill epithelium.Journal of Experimental Biology 161:119–134.

    Google Scholar 

  • Maetz, J. 1971. Fish gills: Mechanisms of salt transfer in freshwater and seawater.Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 262:209–249.

    Article  CAS  Google Scholar 

  • Maetz, J., N. Mayer, andM. M. Charatier-Baraduc. 1967a. La balance minérale du sodium chezAnguilla anguilla en eau de mer, en eau douce et au cours de transfert d’un milieu à l’autre: Effects de l’hypophysectomie et de la prolactine.General and Comparative Endocrinology 8:177–188.

    Article  CAS  Google Scholar 

  • Maetz, J., W. H. Sawyer, G. E. Pickford, andN. Mayer. 1967b. Evolution de la balance minérale du sodium chezFundulus heteroclitus au cours du transfert d’eau de mer d’eau douce: Effets, du hypophysectomie et de la prolactine.General and Comparative Endocrinology 8:163–176.

    Article  CAS  Google Scholar 

  • Marshall, W. S. 1977. Transepithelial potential and short-circuit current across the isolated skin ofGillichthys mirabilis (Teleostei: Gobiidae) acclimated to 5% and 100% seawater.Journal of Comparative Physiology 114:157–165.

    Google Scholar 

  • Marshall, W. S. 1981a. Sodium dependency of active chloride transport across isolated fish skin (Gillichthys mirabilis).Journal of Physiology 319:165–178.

    CAS  Google Scholar 

  • Marshall, W. S. 1981b. Active transport of Rb+ across the skin of the teleostGillichthys mirabilis.American Journal of Physiology 241:F482-F486.

    CAS  Google Scholar 

  • Marshall, W. S. 1985. Paracellular ion transport in trout opercular epithelium models osmoregulatory effects of acid precipitation.Canadian Journal of Zoology 63:1816–1822.

    Article  CAS  Google Scholar 

  • Marshall, W. S. andH. A. Bern. 1979. Teleostean urophysis: Urotensin II and ion transport across the isolated skin of a marine teleost.Science 204:519–521.

    Article  CAS  Google Scholar 

  • Marshall, W. S. andH. A. Bern. 1980. Ion transport across the isolated skin of the teleostGillichthys mirabilis. p. 337–350.In B. Lahlou (ed.), Epithelial Transport in the Lower Vertebrates. Cambridge University Press, Cambridge.

    Google Scholar 

  • Marshall, W. S. andJ. W. Hanrahan. 1991. Anion channels in the apical membrane of mammalian corneal epithelium primary cultures.Investigative Ophthalmology and Visual Sciences 32:1562–1568.

    CAS  Google Scholar 

  • Marshall, W. S. andR. S. Nishioka. 1980. Relation of mitochondria-rich chloride cells to active chloride transport in the skin of a marine teleost.Journal of Experimental Zoology 214:147–156.

    Article  CAS  Google Scholar 

  • Marshall, W. S., S. E. Bryson, andC. M. Wood. 1992. Calcium transport by isolated skin of rainbow trout.Journal of Experimental Biology 166:297–316.

    CAS  Google Scholar 

  • Mayer-Gostan, N. andJ. Maetz. 1980. Ionic exchanges in the opercular membrane ofFundulus heteroclitus adapted to seawater, p. 233–248.In B. Lahlou (ed.), Epithelial Transport in the Lower Vertebrates. Cambridge University Press, Cambridge.

    Google Scholar 

  • McCormick, S. D. 1991. Cortisol directly stimulates differentiation of chloride cells in tilpia opercular membrane.American Journal of Physiology 259:R857-R863.

    Google Scholar 

  • McCormick, S. D. 1994. The ontogeny of salinity tolerance in anadromous salmonids: Hormones and heterochrony.Estuaries 17:26–33.

    Article  CAS  Google Scholar 

  • McCormick, S. D., S. Hasegawa, andT. Hirano. 1992. Calcium uptake in the skin of a freshwater teleost.Proceedings of the National Academy of Sciences of the U.S.A. 89:3635–3638.

    Article  CAS  Google Scholar 

  • McDonald, D. G., Y. Tang, andR. G. Boutilier. 1989. Acid and ion transfer across the gills of fish: Mechanisms and regulation.Canadian Journal of Zoology 67:3046–3054.

    CAS  Google Scholar 

  • Motais, R., F. Garcia-Romeu, andJ. Maetz. 1966. Exchange diffusion effect and euryhalinity in teleosts.Journal of General Physiology 50:391–442.

    Article  CAS  Google Scholar 

  • Nonnotte, G., L. Nonnotte, andR. Kirsch. 1979. Chloride cells and chloride exchange in the skin of a sea-water teleost, the shanny (Blennius pholis L.).Cell and Tissue Research 199: 387–396.

    Article  CAS  Google Scholar 

  • Pang, P. K. T. andR. K. Pang. 1986. Hormones and calcium regulation inFundulus heteroclitus.American Zoologist 26:225–234.

    Google Scholar 

  • Payan, P., J. P. Girard, andN. Mayer-Gostan. 1984. Branchial ion movements in teleosts; the roles of respiratory and chloride cells.In D. J. Randall and W. S. Hoar (eds.), Fish Physiology, Vol. 10B. Academic Press, Orlando, Florida.

    Google Scholar 

  • Péqueux, A., R. Gilles, andW. S. Marshall. 1988. NaCl transport in gills and related structures, p. 1–73.In R. Greger (ed.), Advances in Comparative and Environmental Physiology, Vol. I. Springer-Verlag, Heidelberg.

    Google Scholar 

  • Perry, S. F. andG. Flik. 1988. Characterization of branchial transepithelial calcium fluxes in the freshwater trout (Salmo gairdneri).American Journal of Physiology 254:R491-R498.

    CAS  Google Scholar 

  • Perry, S. F. andP. Laurent. 1989. Adaptational responses of rainbow trout to lowered external NaCl: Contribution to the branchial chloride cell.Journal of Experimental Biology 147:147–168.

    CAS  Google Scholar 

  • Perry, S. F. andC. M. Wood. 1985. Kinetics, of branchial calcium uptake in the rainbow trout: Effects of acclination to various external calcium levels.Journal of Experimental Biology 116:411–433.

    Google Scholar 

  • Pettengill, O. andD. E. Copeland. 1948. alkaline phosphatase activity in the chloride cell ofFundulus heteroclitus and its relation to osmotic work.Journal of Experimental Zoology 108:235–242.

    Article  CAS  Google Scholar 

  • Philpott, C. W. 1965. Halide localization in the teleost chloride cell and its identification by selected area electron diffraction. Direct evidence supporting an osmoregulatory function for the seawater adapted chloride cell ofFundulus.Protoplasma 60:7–23.

    Article  CAS  Google Scholar 

  • Philpott, C. W. 1966. The use of the horseradish peroxidase to demonstrate functional continuity between the plasmalemma and the unique tubular system of the chloride cell.Journal of Cell Biology 31:86.

    Google Scholar 

  • Philpott, C. W.. 1980. Tubular system membranes of teleost chloride cells: Osmotic response and transport sites.American Journal of Physiology 238:R171-R184.

    CAS  Google Scholar 

  • Philpott, C. W. andD. E. Copeland. 1963. Fine structure of chloride cells from three species ofFundulus.Journal of Cell Biology 18:389–404.

    Article  CAS  Google Scholar 

  • Pic, P. 1978. A comparative study of the mechanism of Na+ and Cl− excretion by the gill ofMugil capito andFundulus heteroclitus. Effects of stress.Journal of Comparative Physiology 123:155–162.

    CAS  Google Scholar 

  • Pickford, G. E., R. W. Griffith, J. Torretti, E. Hendlez, andF. H. Epstein. 1970a. Branchial reduction and renal stimulation of (Na+, K+)-ATPase by prolactin in hypophysectomized killifish in freshwater.Nature 228:378–379.

    Article  CAS  Google Scholar 

  • Pickford, G. E., P. K. T. Pang, andW. H. Sawyer. 1966. Prolactin and serum osmolatity of hypophysectomized killifish,Fundulus heteroclitus, in freshwater.Nature 209:1041–1042.

    Article  Google Scholar 

  • Pickford, G. E., P. K. T. Pang, E. Weinstein, J. Torretti, E. Hendler, andF. H. Epstein. 1970b. Response of the hypophysectomized cyprinodontFundulus heteroditus to replacement therapy with cortisol: Effects on blood serum and sodium-potassium activated adenosine triphosphatase in the gills, kidney, and intestinal mucosa.General and Comparative Endocrinology 14:524–534.

    Article  CAS  Google Scholar 

  • Pickford, G. E. andJ. G. Phillips. 1959. Prolactin, a factor promoting survival of hypophysectomized killifish in fresh water.Science 130:454–455.

    Article  CAS  Google Scholar 

  • Potts, W. T. W. 1984. Trans-epithelial potentials in fish gills, p. 105–128.In W. S. Hoar and D. J. Randall (eds.), Fish Physiology, Volume 10B. Academic Press, Orlando, Florida.

    Google Scholar 

  • Potts, W. T. W. andF. B. Eddy. 1973. Gill potentials and sodium fluxes in the flounderPlatichthys flesus.Journal of Comparative Physiology 87:29–48.

    Article  Google Scholar 

  • Potts, W. T. W. andD. H. Evans. 1966. The effects of hypophysectomy and bovine prolactin on salt fluxes in freshwater-adaptedFundulus heteroclitus.Biological Bulletin 131:362–368.

    Article  CAS  Google Scholar 

  • Potts, W. T. W. andD. H. Evans. 1967. Sodium and chloride balance in the killifishFundulus heteroditus.Biological Bulletin 133:411–425.

    Article  CAS  Google Scholar 

  • Potts, W. T. W. andW. R. Fleming. 1971. The effect of environmental calcium and ovine prolactin on sodium balance inFundulus kansae.Journal of Experimental Biology 54:63–75.

    Google Scholar 

  • Ritch, R. andC. W. Philpott. 1969. Repeating particles associated with an electrolyte transport membrane.Experimental Cell Research 55:17–24.

    Article  CAS  Google Scholar 

  • Samaritan, J. M. andR. E. Schmidt. 1982. Aspects of the life history of a freshwater population of the mummichog,Fundulus heteroclitus (Pisces: Cyprinodontidae), in the Bronx River, New York, U.S.A..Hydrobiologia 94:149–154.

    Google Scholar 

  • Sardet, C., M. Pisam, andJ. Maetz. 1979. The surface epithelium of teleostean fish gills: Cellular and junctional adaptations of the chloride cell in relation to salt adaptation.Journal of Cell Biology 80:96–117.

    Article  CAS  Google Scholar 

  • Scheffey, C., J. K. Foskett, andT. E. Machen. 1983. Localization of ionic pathways in the teleost opercular membrane by extracellular recording with a vibrating probe.Journal of Membrane Biology 75:193–203.

    Article  CAS  Google Scholar 

  • Scott, W. B. and M. G. Scott. 1988. Atlantic fishes of Canada.Canadian Bulletin of Fisheries and Aquatic Sciences 219:731 p.

    Google Scholar 

  • Silva, P., R. Solomon, K. Spokes, andF. H. Epstein. 1977. Ouabain inhibition of gill Na+−K+-ATPase: Relationship to active chloride transport.Journal of Experimental Zoology 199:419–426.

    Article  CAS  Google Scholar 

  • Smith, H. W.. 1930. The absorption and excretion of water and salts by marine teleosts.American Journal of Physiology 93:485–505.

    Google Scholar 

  • Stanley, J. G. andW. R. Fleming. 1964. Excretion of hypertonic urine by a teleost.Science 144:63–64.

    Article  Google Scholar 

  • Stanley, J. G. andW. R. Fleming. 1966. The effect of hypophysectomy on sodium metabolism of the gill and kidney ofFundulus kansae.Biological Bulletin 131:155–165.

    Article  CAS  Google Scholar 

  • Stanley, J. G. andW. R. Fleming. 1967. Effect of prolactin and ACTH on the serum and urine sodium levels ofFundulus kansae.Comparative Biochemistry and Physiology 20:199–208.

    Article  CAS  Google Scholar 

  • Stewart, P. A. 1983. Modern quantitative acid-base chemistry.Canadian Journal of Physiology and Pharmacology 61:1444–1461.

    CAS  Google Scholar 

  • Tabcharani, J. A., T. J. Jensen, J. R. Riordan, andJ. W. Hanrahan. 1990. Bicarbonate permeability of the outwardly rectifying anion channel.Journal of Membrane Biology 112:109–122.

    Google Scholar 

  • Taylor, M. H., L. DiMichele, andG. J. Leach. 1977. Egg stranding in the life cycle of the mummichog,Fundulus heteroclitus.Copeia 1977:397–399.

    Article  Google Scholar 

  • Thompson, R. A. 1972. Mechanisms of osmoregulation in a euryhaline goby,Gillichthys mirabilis. The role of active and passive transport of sodium and chloride across the gills. Ph.D. Dissertation, University of California, San Diego, California. 105 p.

    Google Scholar 

  • Towle, D. W., M. E. Gilman, andJ. D. Hempel. 1977. Rapid modulation of gill Na++K+-dependent ATPase activity during acclimation of the killifishFundulus heteroclitus to salinity change.Journal of Experimental Zoology 202:179–186.

    Article  CAS  Google Scholar 

  • Ussing, H. H. 1949. The distinction by means of tracers between active transport and diffusion.Acta Physiologica Scandanavica 19:43–56.

    Article  CAS  Google Scholar 

  • Welsh, M. J. andC. M. Liedke. 1986. Chloride and potassium channels in cystic fibrosis airway epithelia.Nature 322:467–470.

    Article  CAS  Google Scholar 

  • Wood, C. M. 1991. Branchial ion and acid-base transfer in freshwater teleost fish: Environmental hyperoxia as a probe.Physiological Zoology 64:68–102.

    Google Scholar 

  • Zadunaisky, J. A. 1984. The chloride cell: The active transport of chloride and the paracellular pathways, p. 129–170.In W. S. Hoar and D. J. Randall (eds.), Fish Physiology, Vol. 10B. Academic Press, Orlando, Florida.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, McMaster University, L8S 4K1, Hamilton, Ontario, Canada

    Chris M. Wood

  2. Department of Biology, St. Francis Xavier University, B2G 2W5, Antigonish, Nova Scotia, Canada

    William S. Marshall

Authors
  1. Chris M. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William S. Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wood, C.M., Marshall, W.S. Ion balance, acid-base regulation, and chloride cell function in the common killifish,Fundulus heteroclitus—a euryhaline estuarine teleost. Estuaries 17, 34–52 (1994). https://doi.org/10.2307/1352333

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.2307/1352333

Keywords

Search

Navigation