Abstract
Light and election microscopy were used to document the degree of renal corpuscle development in boreal telcost fishes that produce peptide or glycopeptide antifreeze compounds on a seasonal or permanent basis. Emphasis was placed on gadids, cottids and pleuronectids from both the North Atlantic and North Pacific Oceans. Based on the classification of Marshall and Smith (1930), corpuscle development ranged from fully glomerular (Type 1) to pauciglomerular (Type III). Unlike the situation in Antarctic notothenioid fishes, there were no aglomerular species among the boreal fishes. Corpuscles were small in diameter in gadids whereas in cottids they ranged from small to large with considerable intraspecific variation. Eight of eleven species with antifreeze had intermediate (Type II–III) or pauciglomerular kidneys with relatively few dense corpuscles (dia. 36–82μm). In some of these species an extensive mesangium and a substantial capillary endothelium contributed to a glomerular filtration barrier that was four to five times thicker than that in Type I kidneys. The corpuscles of other pauciglomerular species were unremarkable and appeared functional at the ultrastructural level. The boreal fish fauna is taxonomically diverse and, compared to the unrelated Antarctic fauna, of relatively recent evolutionary origin. Furthermore, antifreeze is present only during the winter in some species. Hence it is not surprising that the urinary conservation of antifreeze is accomplished by mechanisms other than the evolutionary loss of renal corpuscles.
Similar content being viewed by others
References cited
Andriyashev, A.P. 1954. Fishes of the Northern Seas of the U.S.S.R. Israel Program for Scientific Translations, Jerusalem.
Bigelow, H.B. and Schroeder, W.C. 1953. Fishes of the Gulf of Maine. U.S. Government Printing Office. Washington.
Boyd, R.B. and DeVries, A.I. 1983. The seasonal distribution of anionie binding sites in ihe basement membrane of the kidney glometulus of the winter flounderPseudopleuronectes americanus. Cell Liss. Res. 234: 271–277.
Boyd, R.B. and DeVries, A.I. 1986. A eomparison ol anionie sites in the glomerular basement membranes from different classes of fishes. Cell Fiss. Res. 245: 513–517.
Bulger, R.I. and Dobyan, D.C. 1982. Recent advanees in renal morphology. Ann. Rev. Physiol. 44: 147–179.
Bulger, R.E. and Trump, B.F. 1968. Renal morphology of the English sole (Parophrys vetulus). Am. J. Anal. 123: 195–226.
Colville, I.P., Richards, R.H. and Dobbie, J.W. 1983. Variations in renal corpuscular morphology with adaptation to seawater in the rainbow trout.Salma gairdneri Richardson. J. Fish Biol. 23: 451–456.
De Ruiter, A.J.H. 1981. Testosterone-dependent changesin vivo andin vitro in the structure of the renal glomeruli of the teleostGasterosteus aculeatus I. Cell Tiss. Res. 219: 253–266.
DeVries, A.I. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172: 1152–1155.
DeVries, A.L. 1980. Biological antifreezes and survival in freezing environments.In Animals and Environmental Fitness. pp. 583 607. Edited by R. Gilles. Pergamon Press, Oxford.
DeVries, A.I. 1982. Biological antifreeze agents in coldwaler fishes. Comp. Biochem. Physiol. 73A: 627–640.
DeVries, A.I. 1993. Antifreeze peptides and glycopeptides in cold-water fishes. Ann. Rev. Physiol. 45: 245–260.
DeVries, A.L. 1986. Antifreeze glycopeptides and peptides: Interactions with ice and water. Meth. Enzymol. 127: 293–303.
DeWitt, H.H. 1971. Coastal and deep-water benthie fishes of the Antarctic. Antarct. Map Folio Ser. 15: 1–10.
Dobbs, G.H., III and DeVries, A.L. 1975a. The aglomerular nephron of Antarctic teleosts: A light and electron microscopic study. Tiss. Cell 7: 159–170.
Dobbs, G.H., III and DeVries, A.L. 1975b. Renal function in Antarctic teleost fishes: Serum and urine composition. Mar. Biol. 29: 59–70.
Dobbs, G.H., III, Lin, Y. and DeVries, A.L. 1974. Aglomerularism in Antarctic fish. Science 185: 793–794.
Duman, J.G. and DeVries, A.L. 1975. The role of macromolecular antifreezes in cold water fishes. Comp. Biochem. Physiol. 52A: 193–199.
Eastman, J.T. and DeVries, A.L. 1986. Renal glomerular evolution in Antarctic notothenioid fishes. J. Fish Biol. 29: 649–662.
Eastman, J.T., DeVries, A.L., Coalson, R.E., Nordquist, R.E. and Boyd, R.B. 1979. Renal conservation of antifreeze peptide in Antarctic celpout.Rhigophila dearborm. Nature. Lond. 282: 217–218.
Elger, M., Kaune, R. and Hentschel, H. 1984. Glomerular intermittency in a freshwater teleost.Carassius auratus gibelio, after transfer to salt water. J. Comp. Physiol. B 154: 225–231.
Forster, R.P. 1953. A comparative study of renal function in marine telcosts. J. Cell. Comp. Physiol. 42: 487–509.
Forster, R.P. 1975. Structure and function of aglomerular kidneys. Fortschr. Zool. 23: 232–247.
Grafflin, A.L. 1933. Glomerular degeneration in the kidney of the daddy seulpin (Myoxocephalus scorpius). Anal. Rec. 57: 59–79.
Grande, I. and Eastman, J.I. 1986. A review of Antarctic ichthyofaunas in the light of new fossil discoveries. Palacontology 29: 113–137.
Hickman, C.P., Jr. 1968. Glomerular filtration and urine flow in the euryhaline southern flounder.Paralichthys lethostigma. in seawater. Can. J. Zool. 46: 427–437.
Hickman, C.P., Jr. and Trump, B.F. 1969. The kidney.In Fish' Physiology, Vol. 1. pp. 91–239. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.
Hubbs, C.I., and Hubbs, C. 1953. An improved graphical analysis and comparison of series of samples. Syst. Zool. 2: 49–57.
Johnson, G.I., Vanney, J.R. and Hayes, D. 1982. The Antarctic continental shell.In Antarctic Geoscience. pp. 995–1002. Edited by C. Craddock. University of Wisconsin Press, Madison.
Kanwar, Y.S. and Farquhar, M.G. 1979. Presence of heparan sulfate in the glomerular basement membrane. Proc. Natl. Acad. Sci. U.S.A. 76: 1303–1307.
Kanwar, Y.S., Linker, A. and Farquhar, M.G. 1980. Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion. J. Cell Biol. 86: 688–693.
Kao, M.H., Fletcher, G.I., Wang, N.C. and Hew, C.I. 1986. The relationship between molecular weight and antifreeze polypeptide activity in marine fish. Can. J. Zool. 64: 578–582.
Leim, A.H. and Scott, W.B. 1966. Fishes of the Atlantic Coast of Canada. Fisheries Research Board of Canada, Bull. No. 155, Ottawa.
Llano, G.A. 1978. Polar research: A synthesis with special reference to biology.In Polar Research: To the Present, and the Future, pp. 27–61. Edited by M.A. McWhinnie. Westview Press, Boulder, Colorado.
Marshall, E.K., Jr. and Smith, H.W. 1930. The glomerular development of the vertebrate kidney in relation to habilat. Biol. Bull. 59: 135–153.
Morrow, J.E. 1980. The Freshwater Fishes of Alaska. Alaska Northwest Publishing Co., Anchorage.
Nash, J. 1931. The number and size of glomeruli in the kidneys of fishes. with observations on the morphology of the renal tubules of fishes. Am. J. Anal. 47: 425–445.
O'Grady, S.M., Schrag, J.D., Raymond, J.A. and DeVries, A.L. 1982. Comparison of antifreeze glycopeptides from Arctic and Antarctic fishes. J. Exp. Zool. 224: 177–185.
Petzel, D.H. 1982. Circulatory Conservation of Anionic Antifreeze Peptides in the Glomerular Winter Flounder (Pseudopleuronectes americanus). Ph.D. Thesis, University of Illinois at Urbana-Champaign.
Raymond, J.A., Lin, Y. and DeVries, A.L. 1975. Glycoprotein and protein antifreezes in two Alaskan fishes. J. Exp. Zool. 193: 125–130.
Renkin, E.M. and Gilmore, J.P. 1973. Glomerular filtration.In Handbook of Physiology, Section 8: Renal Physiology, pp. 185–248. Edited by J. Orloff and R.W. Berliner. American Physiological Society, Washington.
Rhodin, J.A.G. 1974. Histology: A Text and Atlas. Oxford University Press, New York.
Simpson, G.G., Row, A. and Lewontin, R.C. 1960. Quantitative Zoology (revised edition). Harcourt, Brace & World, New York.
Sokal, R.R. and Rohlf, F.J. 1981. Biometry (2nd ed.). Freeman, San Francisco.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Eastman, J.T., Boyd, R.B. & DeVries, A.L. Renal corpuscle development in boreal fishes with and without antifreezes. Fish Physiol Biochem 4, 89–100 (1987). https://doi.org/10.1007/BF02044318
Issue Date:
DOI: https://doi.org/10.1007/BF02044318