Abstract
Renal function was observed in freshwater North American eels (Anguilla rostrata LeSueur) 2 weeks after the removal of the corpuscles of Stannius. There was a positive linear correlation between glomerular filtration rates and urine flow rates in both sham-operated and stanniectomized eels but there was no difference in slope or elevation between the two groups nor did urine flow rates ever exceed glomerular filtration rates. Osmolar clearance and free-water clearance were unchanged following stanniectomy. Plasma Ca2+ and K+ concentrations increased and plasma Mg2+, phosphate, Na+ and Cl- concentrations decreased following stanniectomy. Plasma ultrafilterable Ca increased and ultrafilterable Mg decreased after stanniectomy but neither changed relative to its total plasma concentration. Stanniectomy was followed by a decreased renal tubular reabsorption of Mg2+ relative to the amount filtered (C Mg/C In); the same applies to C Na/C In. Even though the filtered load of Ca increased in conjuction with the predictable hypercalcemia, there was no change in the fraction of filtered Ca reabsorbed. Net tubular secretion of phosphate was observed in both sham-operated and stanniectomized cels together with a slight increase in C phos/C In following stanniectomy. Some or all of these changes in plasma electrolytes and/or the modified renal transport of Na+, Mg2+ and possibly phosphate may be caused by the changes in cardiovascular function that were recently shown to follow stanniectomy.
Similar content being viewed by others
Abbreviations
- CSX :
-
Stanniectomized/stanniectomy
- ER :
-
endoplasmatic reticulum
- FW :
-
fresh water
- GFR :
-
glomerular filtration rate
- Pi :
-
inorganic phosphate
- RAS :
-
renin-angiotensin system
- SHM :
-
sham-operated
- SW :
-
sea water
- UFR :
-
urine flow rate
- U/P ratio :
-
urine/plasma ratio
References
Babiker MM, Rankin JC (1978) Neurohypophysial hormonal control of kidney function in the European eel (Anguilla anguilla L.) adapted to sea water or fresh water. J Endocrinol 76:347–358
Beyenbach KW, Kirschner LB (1976) The unreliability of mammalian glomerular markers in teleostean renal studies. J Exp Biol 64:369–378
Butler DG (1969) Corpuscles of Stannius and renal physiology in the eel (Anguilla rostrata). J Fish Res Board Can 26:639–654
Butler DG (1972) Failure to observe changes in selected metabolites following removal of the Stannius corpuscles from the freshwater North American eel, Anguilla rostrata. J Fish Res Board Can 29: 1362–1364
Butler DG (1993) Stanniectomy increases renal magnesium and calcium excretion in freshwater North American eels (Anguilla anguilla L.). J Exp Biol 181:107–118
Butler DG, Oudit GY (1995) Dorsal aortic and organ blood flow decrease following stanniectomy of freshwater North American eels (Anguilla rostrata LeSueur). Comp Biochem Physiol 108A:229–238
Butler DG, Oudit GY (1995) Corpuscles of Stannius and blood flow regulation in freshwater North American els, Anguilla rostrata LeSueur. J Endocrinol 145:181–194
Chan DKO (1968) Endocrine regulation of calcium and inorganic phosphate balance in the freshwater-adapted teleost fish, Anguilla anguilla and A. japonica. Proceedings of the Third International Congress of Endocrinology, Mexico City. International Congress Series. Excerpta Med 184:709–716
Chan DKO, Chester Jones I (1968) Regulation and distribution of plasma calcium and inorganic phosphate in the European eel (Anguilla anguilla L.). J Endocrinol 42:109–117
Chan DKO, Chester Jones I, Henderson IW, Rankin JC (1967) Studies on the experimental alteration of water and electrolyte composition of the eel (Anguilla anguilla L.). J Endocrinol 37 297–317
Chan DKO, Rankin JC, Chester Jones I (1969) Influences of the adrenal cortex and the corpuscles of Stannius on osmoregulation in the European eel (Anguilla anguilla L.) adapted to freshwater. Gen Comp Endocrinol [Suppl] 2:342–353
Chester Jones I, Chan DKO, Rankin JC (1969) Renal function in the European eel (Anguilla anguilla L.): effects of the caudal neurosecretory system, corpuscles of Stannius, neurohypophysial peptides and vasoactive substances. J Endocrinol 43:21–31
Chester Jones I, Henderson IW, Chan DKO, Rankin JC, Mosley W, Brown JJ, Lever AF, Robertson JIS, Tree M (1966) Pressor activity in extracts of the corpuscles of Stannius from the European eel (Anguilla anguilla L.). J Endocrinol 34: 393–408
Clarke RW, Smith HW (1932) Absorption and excretion of water and salts by the elasmobranch fishes. III. The use of xylose as a measure of the glomerular filtrate in Squalus acanthias. J Cell Comp Physiol 1:131–143
Dantzler WH (1985) Comparative aspects of renal function. In: Seldin DW (ed) The kidney: physiology and pathophysiology, vol 1. Raven Press, New York, pp 333–364
Fenwick JC (1974) The corpuscles of Stannius and calcium regulation in the North American eel (Anguilla rostrata LeSueur). Gen Comp Endocrinol 23:127–135
Fenwick JC (1989) Calcium exchange across fish gills. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 3. Academic Press, San Diego, pp 319–336
Fenwick JC, So YP (1974) A perfusion study of the effect of Stanniectomy on the net influx of calcium-45 across an isolated eel gill. J Exp Zool 188:125–131
Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375
Fontaine M (1964) Corpuscules de Stannius et régulation ionique (Ca, K et Na) du milieu intérieur de l'anguille (Anguilla anguilla L.). C r hebd Séances Acad Sci, Paris 259:875–878
Fontaine M (1967) Intervention des corpuscules de Stannius dans l'équilibre phosphocalcique du milieu intérieur d'un poisson téléostéen l'Anguilla. C r hedb Séances acad Sci, Paris 264: 736–737
Fontaine M, Delerue N, Martelly E, Marchelidon J, Milet C (1972) Róle des corpuscules de Stannius dans les échanges de calcium d'un poisson téléostéen, L'anguille (Anguilla anguilla), avec le milieu ambiant. C R Acad Sci, Paris 275:1523–1528
Ford P (1959) Some observations on the corpuscles of Stannius. In: Gorbman A (ed) Comparative endocrinology. Wiley, New York, pp 728–734
Gallardy R, Podhasky P, Olson KR (1984) Angiotensin-converting enzyme activity in tissues of the rainbow trout. J Exp Zool 230: 155–158
Galli-Gallardo SM, Marusic ET, Pang PKT (1977) Studies on the Stannius corpuscles of the Chilcan clingfish, Sicyases sanguineus. Gen Comp Endocrinol 32:316–320
Garrett FD (1942) The development and phylogeny of the corpuscles of Stannius in ganoid and teleostean fishes. J Morphol 70:41–67
Gupta A, Renfro JL (1991) Effects of pH on phosphate transport by flounder renal tubule primary cultures. Am J Physiol 260: R704-R711
Hanssen RGJM, Lafeber FPJG, Flik G, Wendelaar Bonga SE (1989) Ionic and total calcium levels in the blood of the European eel (Anguilla anguilla): effects of Stanniectomy and hypocalcin replacement therapy. J Exp Biol 141:189–191
Harris CA, Sutton RAL, Dirks JH (1977) Effects of hypercalcemia on calcium and phosphate ultrafilterability and tubular reabsorption in the rat. Am J Physiol 233:F201-F206
Hirano T (1989) The corpuscle of Stannius. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 3. Academic Press, San Diego, pp 139–170
Huot E (1898) Préliminaire sur l'origine des canpsules surrénales des poissons Lophobranches. C R Acad Sci, Paris 126:49–50
Ichikawa I, Brenner BW (1976) Of unglazed pottery and glomerular sieving. Kidney Int 10:246–267
Kaune R, Hentschel H (1987) Stimulation of renal phosphate secretion in the stenohaline freshwater teleost: Carassius auratus gibelio Bloch. Comp Biochem Physiol 87A:359–362
Kenyon CJ, Chester Jones I, Dixon RNB (1980) Acute responses of the freshwater eel (Anguilla anguilla) to extracts of the corpuscles of Stannius opposing the effects of stanniosomatiectomy. Gen Comp Endocrinol 41:531–538
Massry SG, Coburn JW, Kleeman CR (1969) Renal handling of magnesium in the dog. Am J Physiol 216:1460–1467
Meats M, Ingleton PM, Chester Jones I, Garland HO, Kenyon CJ (1978) Fine structure of the corpuscles of Stannius of the trout, Salmo gairdneri: structural changes in response to increased environmental salinity and calcium ions. Gen Comp Endocrinol 36:451–461
Ogawa M (1968) Osmotic and ionic regulation in goldfish following removal of the corpuscles of Stannius or the pituitary gland. Can J Zool 46:669–676
Oikari AOJ, Rankin JC (1985) Renal excretion of magnesium in a freshwater teleost, Salmo gairneri. J Exp Biol 117:319–333
Pang PKT (1971) The relationship between corpuscles of Stannius and serum electrolyte regulation in kilifish, Fundulus heteroclitus. J Exp Biol 178:1–8
Pang PKT (1973) Endocrine control of calcium metabolism in teleosts. Am Zool 13:775–792
Pang PKT, Pang RK, Sawyer WH (1973) Effects of environmental calcium and replacement therapy on the killifish, Fundulus heteroclitus, after surgical removal of the corpuscles of Stannius. Endocrinology (Baltimore) 93:705–710
Pang PKT, Pang RK, Sawyer WH (1974) Environmental calcium and the sensitivity of killifish (Fundulus heteroclitus) in bioassays for the hypocalcemic response to Stannius corpuscles from killifish and cod (Gadus morhua). Endocrinology (Baltimore) 94:548–555
Rankin JC (1967) Studies on the endocrine control of osmoregulation in the eel, Anguilla anguilla L. Ph.D. thesis, University of Sheffield, England, 141 pp
Rankin JC, Chan DKO, Chester Jones I (1967) Kidney function in the European eel, Anguilla anguilla. Gen Comp Endocrinol 9: 484–485
Rankin JC, Wahlqvist I, Wallace B (1984) Antidiurectic actions of angiotensin II, catecholamines and neurohypophysial hormones in the in situ perfused rainbow trout kidney. Gen Comp Endocrinol 53:442
Renkin EM, Gilmore JP (1973) Glomerular filtration. In: Orloff J, Berlinger RW (eds) Handbook of physiology: renal physiology, sect 8. American Physiological Society, Washington, DC, pp 185–248
Renfro LJ (1980) Relationship between renal fluid and Mg secretion in a glomerular marine teleost. Am J Physiol 238: F92-F98
Schmidt-Nielsen B, Renfro JL (1975) Kidney function of the American eel, Anguilla rostrata. Am J Physiol 228:420–431
So YP, Fenwick JC (1979) In vivo and in vitro effects of Stannius corpuscle extract on the branchial uptake of 45Ca in stanniectomized North American eel (Anguilla rostrata). Gen Comp Endocrinol 37:143–149
Stannius H (1839) Die Nebennieren bei Knochenfischen. Arch Anat Physiol 8:223–271
Stolte H, Galaske RG, Eisenbach GM, Lechene C, Schmidt-Nielsen B, Boyland JW (1977) Renal tubule ion transport and collecting duct function in the elasmobranch little skate, Raja erinacea. J Exp Biol 199:403–410
Takagi Y, Nakamura Y, Yamada J (1985) Effects of the removal of the corpuscles of Stannius on the transport of calcium across the intestine of rainbow trout. Zool Sci (Tokyo) 6:83–89
Takemoto Y, Nakajima T, Hasegawa Y, Watanabe TX, Sokabe H, Kumagae S, Sakakibara S (1983) Chemical structure of angiotensin formed by incubating plasma with the kidney and the corpuscles of Stannius in the chum salmon, Oncorhynchus keta. Gen Comp Endocrinol 51:219–227
Telford IR, Bridgman CF (1990) Introduction to functional histology. Harper and Row, New York
Urasa FM, Wendelaar Bonga SE (1987) Effects of calcium and phosphate on the corpuscles of Stannius of the teleost fish, Oreochromis mossambicus. Cell Tissue Res 249:681–690
Verbost PM, Butkus A, Wiliems P, Wendelaar Bonga SE (1993) Indications for two bioactive principles in the corpuscles of Stannius. J Exp Biol 177:243–252
Wagner GF, Fenwick JC, Park CM, Milliken C, Copp DH, Friesen HG (1988) Comparative biochemistry and physiology of teleocalcin from sockeye and coho salmon. Gen Comp Endocrinol 72:237–246
Wagner GF, Hampong M, Park CM, Copp DH (1986) Purification, characterization and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen Comp Endorinol 63:481–491
Walser M (1973) Divalent cations: physicochemical state in glomerular filtrate and urine in renal extraction. In: Orloff J, Berliner RW (eds) Handbook of physiology: renal physiology. Am Physiol Soc, Washinton, DC, pp 555–586
Wearn JT, Richards AN (1925) The concentration of chlorides in the glomerular urine of frogs. J Biol Chem 66:247–273
Wendelaar Bonga SE, Greven JAA (1975) A second cell type in Stannius bodies of two euryhaline teleost species. Cell Tissue Res 159:287–290
Wendelaar Bonga SE, Greven JAA (1978) The relationship between prolactin cell activity, environmental calcium, and plasma calcium in the teleost Gasterosteus aculeatus. Observation on stanniectomized fish. Gen Comp Endocrinol 36: 90–101
Wendelaar Bonga SE, Pang PKT (1986) Stannius corpuscles. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 1. Academic Press, Orlando, pp 439–464
Wendelaar Bonga SE, Van der Meij JCA, Pang PKT (1980) Evidence for two secretory cell types in the Stannius bodies of the teleosts Fundulus heteroclitus and Carassius auratus. Cell Tissue Res 212:295–306
Yamada C, Kobayashi H (1987) Immunoreactive angiotensin II in the corpuscles of Stannius of the rainbow trout, Salmo gairdneri. Zool Sci 4:387–390
Yamane S, Iguchi M, Ogasawara T, Nakamura Y (1982) Effects of blockage of exogenous calcium and phosphorus on the calcium regulatory systems in goldfish. Comp Biochem Physiol 72A: 709–713
Author information
Authors and Affiliations
Additional information
Communicted by H. Langer
Rights and permissions
About this article
Cite this article
Butler, D.G., Alia Cadinouche, M.Z. Fractional reabsorption of calcium, magnesium and phosphate in the kidneys of freshwater North American eels (Anguilla rostrata LeSueur) following removal of the corpuscles of Stannius. J Comp Physiol B 165, 348–358 (1995). https://doi.org/10.1007/BF00387305
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00387305