Abstract
We investigated the transepithelial potential (TEP) and its responses to changes in the external medium in Alcolapia grahami, a small cichlid fish living in Lake Magadi, Kenya. Magadi water is extremely alkaline (pH = 9.92) and otherwise unusual: titratable alkalinity (290 mequiv L−1, i.e. HCO3 − and CO3 2−) rather than Cl− (112 mmol L−1) represents the major anion matching Na+ = 356 mmol L−1, with very low concentrations of Ca2+ and Mg2+ (<1 mmol L−1). Immediately after fish capture, TEP was +4 mV (inside positive), but stabilized at +7 mV at 10–30 h post-capture when experiments were performed in Magadi water. Transfer to 250% Magadi water increased the TEP to +9.5 mV, and transfer to fresh water and deionized water decreased the TEP to −13 and −28 mV, respectively, effects which were not due to changes in pH or osmolality. The very negative TEP in deionized water was attenuated in a linear fashion by log elevations in [Ca2+]. Extreme cold (1 vs. 28°C) reduced the positive TEP in Magadi water by 60%, suggesting blockade of an electrogenic component, but did not alter the negative TEP in dilute solution. When fish were transferred to 350 mmol L−1 solutions of NaHCO3, NaCl, NaNO3, or choline Cl, only the 350 mmol L−1 NaHCO3 solution sustained the TEP unchanged at +7 mV; in all others, the TEP fell. Furthermore, after transfer to 50, 10, and 2% dilutions of 350 mmol L−1 NaHCO3, the TEPs remained identical to those in comparable dilutions of Magadi water, whereas this did not occur with comparable dilutions of 350 mmol L−1 NaCl—i.e. the fish behaves electrically as if living in an NaHCO3 solution equimolar to Magadi water. We conclude that the TEP is largely a Na+ diffusion potential attenuated by some permeability to anions. In Magadi water, the net electrochemical forces driving Na+ inwards (+9.9 mV) and Cl− outwards (+3.4 mV) are small relative to the strong gradient driving HCO3 − inwards (−82.7 mV). Estimated permeability ratios are P Cl/P Na = 0.51–0.68 and \( P_{{{\text{HCO}}_{3} }} /P_{\text{Na}} \) = 0.10–0.33. The low permeability to HCO3 − is unusual, and reflects a unique adaptation to life in extreme alkalinity. Cl− is distributed close to Nernst equilibrium in Magadi water, so there is no need for lower P Cl. The higher P Na likely facilitates Na+ efflux through the paracellular pathway. The positive electrogenic component is probably due to active HCO3 − excretion.
References
Bergman AN, Bergman HL, Laurent P, Maina JN, Walsh PJ, Wood CM (1996) Respiratory physiology of the Lake Magadi tilapia (Oreochromis alcalilcus grahami), a fish adapted to a hot, alkaline, and frequently hypoxic environment. Physiol Zool 69:1114–1136
Bergman AN, Laurent P, Otiang’a-Owiti G, Bergman HL, Walsh PJ, Wilson P, Wood CM (2003) Physiological adaptations of the gut in the Lake Magadi tilapia, Alcolapia grahami, an alkaline- and saline-adapted fish. Comp Biochem Physiol 136A:701–715
Coe MJ (1966) The biology of Tilapia grahami Boulenger in Lake Magadi, Kenya. Acta Trop 23:146–177
Eddy FB (1975) The effect of calcium on gill potentials and on sodium and chloride fluxes in the goldfish, Carassius auratus. J Comp Physiol 96:131–142
Eddy FB, Maloiy GMO (1984) Ionic content of body fluids and sodium efflux in Oreochromis alcalicus grahami, a fish living at temperatures above 30°C and in conditions of extreme alkalinity. Comp Biochem Physiol A 78:359–361
Eddy FB, Bamford OS, Maloiy GMO (1981) Na+ and Cl− effluxes and ionic regulation in Tilapia grahami, a fish living in conditions of extreme alkalinity. J Exp Biol 91:35–349
Goldman DE (1943) Potential, impedance, and rectification in membranes. J Gen Physiol 27:37–60
Hills AG (1973) Acid–base balance; chemistry, physiology, pathophysiology. Williams and Wilkins, Baltimore
House CR, Maetz J (1974) On the electrical gradient across the gill of the seawater adapted eel. Comp Biochem Physiol A 47:917–924
Johansen K, Maloiy GMO, Lykkeboe G (1975) A fish in extreme alkalinity. Respir Physiol 24:156–162
Kerstetter TH, Kirschner LB, Rafuse LB (1970) On the mechanisms of sodium ion transport by the irrigated gills of rainbow trout (Salmo gairdneri). J Gen Physiol 56:342–359
Kirschner LB (1970) The study of NaCl transport in aquatic animals. Am Zool 10:365–376
Laurent PL, Maina JN, Bergman HL, Narahara A, Walsh PJ, Wood CM (1995) Gill structure of a fish from an alkaline lake; effect of short-term exposure to neutral conditions. Can J Zool 73:1170–1181
Leatherland JF, Hyder M, Ensor DM (1974) Regulation of plasma Na+ and K+ concentrations in five species of Tilapia fishes. Comp Biochem Physiol A 48:699–710
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. 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
Maloiy GMO, Lykkeboe G, Johansen K, Bamford OS (1978) Osmoregulation in Tilapia grahami: a fish in extreme alkalinity. In: Schmidt-Nielsen K, Bolis L, Maddrell SHP (eds) Comparative physiology: water, ions and fluid mechanics. Cambridge University Press, Cambridge, pp 229–238
Marshall WS (2003) Rapid regulation of NaCl secretion by estuarine teleost fish: coping strategies for short-duration freshwater exposures. Biochim Biophys Acta 1618:95–105
Marshall WS, Duquesnay RM, Gillis JM, Bryson SE, Liedtke CM (1998) Neural modulation of salt secretion in teleost opercular epithelium by alpha2-adrenergic receptors and inositol 1, 4, 5-trisphosphate. J Exp Biol 201:1959–1965
May SA, Degnan KJ (1985) Converging adrenergic and cholinergic mechanisms in the inhibition of Cl− secretion in fish opercular epithelium. J Comp Physiol B156:183–189
McWilliams PG, Potts WTW (1978) The effects of pH and calcium concentrations on gill potentials in the brown trout, Salmo trutta. J Comp Physiol 126:277–286
Mendelsohn SA, Cherksey BD, Degnan KJ (1981) Adrenergic regulation of chloride secretion across the opercular epithelium: the role of cyclic AMP. J Comp Physiol B145:125–135
Pic P (1978) A comparative study of the mechanisms of Na+ and Cl− excretion by the gill of Mugil capito and Fundulus heteroclitus: effects of stress. J Comp Physiol 123:155–162
Pörtner HO, Schulte PM, Wood CM, Schiemer F (2010) Niche dimensions in fishes: an integrative view. Illustrating the role of physiology in understanding ecological realities. Physiol Biochem Zool 83:808–826
Potts WTW (1984) Transepithelial potentials in fish gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10B. Academic Press, Orlando, pp 105–128
Potts WTW, Eddy FB (1973) Gill potentials and sodium fluxes in the flounder Platichthys stellatus. J Comp Physiol 87:20–48
Potts WTW, Hedges AJ (1991) Gill potentials in marine teleosts. J Comp Physiol B161:401–405
Potts WTW, Fletcher CR, Hedges AJ (1991) The in vivo transepithelial potential in a marine teleost. J Comp Physiol B161:393–400
Randall DJ, Wood CM, Perry SF, Bergman HL, Maloiy GMO, Mommsen TP, Wright PA (1989) Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337:165–166
Robinson RA, Stokes RH (1959) Electrolyte solutions. Butterworth, London, p 559
Seegers L, Sonnenberg R, Yamamoto R (1999) Molecular analysis of the Alcolapia flock from Lakes Natron and Magadi, Tanzania and Kenya (Teleostei: Cichlidae), and implications for their systematics and evolution. Ichthyol Explor Freshw 10:175–199
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
Skadhauge E, Lechene CP, Maloiy GMO (1980) Tilapia grahami: role of intestine in osmoregulation under conditions of extreme alkalinity. In: Lahlou B (ed) Epithelial transport in the lower vertebrates. Cambridge University Press, Cambridge, pp 133–142
Sten-Knudsen O (2002) Biological membranes: theory of transport, potentials, and electrical impulses. Cambridge University Press, Cambridge
Wilson PJ, Wood CM, Maina JN, White BN (2000) Genetic structure of Lake Magadi tilapia populations. J Fish Biol 56:590–603
Wilson PJ, Wood CM, Walsh PJ, Bergman AN, Bergman HL, Laurent P, White BN (2004) Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia. Physiol Biochem Zool 77:537–555
Wood CM, Grosell M (2008) A critical analysis of transepithelial potential in intact killifish (Fundulus heteroclitus) subjected to acute and chronic changes in salinity. J Comp Physiol B 178:713–727
Wood CM, Marshall WS (1994) Ion balance, acid-base regulation, and chloride cell function in the common killifish, Fundulus heteroclitus—a euryhaline estuarine teleost. Estuaries 17:34–52
Wood CM, Perry SF, Wright PA, Bergman HL, Randall DJ (1989) Ammonia and urea dynamics in the Lake Magadi tilapia, a ureotelic teleost fish adapted to an extremely alkaline environment. Respir Physiol 77:1–20
Wood CM, Bergman HL, Laurent P, Maina JN, Narahara A, Walsh P (1994) Urea production, acid-base regulation and their interactions in the Lake Magadi tilapia, a unique teleost adapted to a highly alkaline environment. J Exp Biol 189:13–36
Wood CM, Wilson PW, Bergman HL, Bergman AN, Laurent P, Otiang’a-Owiti G, Walsh PJ (2002a) Ionoregulatory strategies and the role of urea in the Magadi tilapia (Alcolapia grahami). Can J Zool 80:503–515
Wood CM, Wilson PW, Bergman HL, Bergman AN, Laurent P, Otiang’a-Owiti G, Walsh PJ (2002b) Obligatory urea production and the cost of living in the Magadi tilapia revealed by acclimation to reduced salinity and alkalinity. Physiol Biochem Zool 75:111–122
Wright PA, Perry SF, Randall DJ, Wood CM, Bergman HL (1990) The effects of reducing water pH on Oreochromis alcalicus grahami, a teleost fish adapted to an extremely alkaline environment. J Exp Biol 151:361–369
Acknowledgments
We are extremely grateful for the kindness, hospitality, and support of the Magadi Soda Company, and particularly the help of John Ndonga and John Kabera. Dishon Muthee and George Muthee provided invaluable logistical assistance. Three anonymous reviewers provided constructive comments. CMW is supported by the Canada Research Chair Program. AB is a Research Fellow from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and supported by the International Canada Research Chair Program from the International Development Research Centre (IDRC, Ottawa, Canada). Funded by an NSERC (Canada) Discovery grant to CMW, a grant from the Brazilian CNPq to AB, and a grant from the National Research Foundation of South Africa to JM.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
Rights and permissions
About this article
Cite this article
Wood, C.M., Bergman, H.L., Bianchini, A. et al. Transepithelial potential in the Magadi tilapia, a fish living in extreme alkalinity. J Comp Physiol B 182, 247–258 (2012). https://doi.org/10.1007/s00360-011-0614-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-011-0614-y